Mitogen-activated protein kinase-activated protein kinase 2 in angiotensin II-induced inflammation and hypertension: Regulation of oxidative stress

Hypertension

Volumn 57, Issue 2, 2011, Pages 245-254

  Ebrahimian, Talin ^a   Li, Melissa Wei ^a   Lemarié, Catherine A ^a   Simeone, Stefania ^a   Pagano, Patrick J ^c   Gaestel, Matthias ^d   Paradis, Pierre ^a   Wassmann, Sven ^a,b   Schiffrin, Ernesto L ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

angiotensin II; arterial; hypertension; MK2; oxidative stress; vascular inflammation

Indexed keywords

ANGIOTENSIN II; CATALASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; SUPEROXIDE; TRANSCRIPTION FACTOR ETS 1; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL REACTIVITY; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; HYPERTENSION; IN VIVO STUDY; INFLAMMATION; MALE; MEAN ARTERIAL PRESSURE; MESENTERIC VEIN; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; WILD TYPE;

ANGIOTENSIN II; ANIMALS; AORTA; BLOOD PRESSURE; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINE CCL2; HYPERTENSION; INFLAMMATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; NADPH OXIDASE; NF-KAPPA B; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SUPEROXIDES; VASCULAR CELL ADHESION MOLECULE-1;

EID: 79551502923     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.110.159889     Document Type: Article

References (54)

1. Chen XL, Tummala PE, Olbrych MT, Alexander RW, Medford RM. Angiotensin II induces monocyte chemoattractant protein-1 gene expression in rat vascular smooth muscle cells. Circ Res. 1998;83: 952-959.
2. Tummala PE, Chen XL, Sundell CL, Laursen JB, Hammes CP, Alexander RW, Harrison DG, Medford RM. Angiotensin II induces vascular cell adhesion molecule-1 expression in rat vasculature: a potential link between the renin-angiotensin system and atherosclerosis. Circulation. 1999;100:1223-1229.
3. Griendling KK, Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept. 2000;91:21-27.
4. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res. 2000;86:494-501.
5. Touyz RM, Cruzado M, Tabet F, Yao G, Salomon S, Schiffrin EL. Redox-dependent MAP kinase signaling by Ang II in vascular smooth muscle cells: role of receptor tyrosine kinase transactivation. Can J Physiol Pharmacol. 2003;81:159-167.
6. Ushio-Fukai M, Alexander RW, Akers M, Griendling KK. p38 Mitogen-activated protein kinase is a critical component of the redox-sensitive signaling pathways activated by angiotensin II. Role in vascular smooth muscle cell hypertrophy. J Biol Chem. 1998;273:15022-15029.
7. Zhang GY, Li X, Yi CG, Pan H, He GD, Yu Q, Jiang LF, Xu WH, Li ZJ, Ding J, Lin DS, Gao WY. Angiotensin II activates connective tissue growth factor and induces extracellular matrix changes involving Smad/ activation and p38 mitogen-activated protein kinase signaling pathways in human dermal fibroblasts. Exp Dermatol. 2009;18:947-953.
8. Lal AS, Clifton AD, Rouse J, Segal AW, Cohen P. Activation of the neutrophil NADPH oxidase is inhibited by SB 203580, a specific inhibitor of SAPK2/p38. Biochem Biophys Res Commun. 1999;259:465-470.
9. Chan SH, Hsu KS, Huang CC, Wang LL, Ou CC, Chan JY. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla. Circ Res. 2005;97:772-780.
10. Ju H, Behm DJ, Nerurkar S, Eybye ME, Haimbach RE, Olzinski AR, Douglas SA, Willette RN. p38 MAPK inhibitors ameliorate target organ damage in hypertension: part 1. p38 MAPK-dependent endothelial dysfunction and hypertension. J Pharmacol Exp Ther. 2003;307:932-938. (Pubitemid 37494209)
11. Komers R, Schutzer W, Xue H, Oyama TT, Lindsley JN, Anderson S. Effects of p38 mitogen-activated protein kinase inhibition on blood pressure, renal hemodynamics, and renal vascular reactivity in normal and diabetic rats. Transl Res. 2007;150:343-349.
12. Clerk A, Michael A, Sugden PH. Stimulation of multiple mitogen-acti-vated protein kinase sub-families by oxidative stress and phosphorylation of the small heat shock protein, HSP25/27, in neonatal ventricular myocytes. Biochem J. 1998;333:581-589.
13. New L, Jiang Y, Zhao M, Liu K, Zhu W, Flood LJ, Kato Y, Parry GC, Han J. PRAK, a novel protein kinase regulated by the p38 MAP kinase. EMBO J. 1998;17:3372-3384. (Pubitemid 28279511)
14. Touyz RM, He G, El Mabrouk M, Schiffrin EL. p38 Map kinase regulates vascular smooth muscle cell collagen synthesis by angiotensin II in SHR but not in WKY. Hypertension. 2001;37:574-580.
15. 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.
16. Fukunaga R, Hunter T. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J. 1997;16:1921-1933.
17. Waskiewicz AJ, Flynn A, Proud CG, Cooper JA. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J. 1997;16:1909-1920.
18. Ben-Levy R, Hooper S, Wilson R, Paterson HF, Marshall CJ. Nuclear export of the stress-activated protein kinase p38 mediated by its substrate MAPKAP kinase-2. Curr Biol. 1998;8:1049-1057.
19. Adams RH, Porras A, Alonso G, Jones M, Vintersten K, Panelli S, Valladares A, Perez L, Klein R, Nebreda AR. Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol Cell. 2000;6:109-116.
20. Chrestensen CA, Schroeder MJ, Shabanowitz J, Hunt DF, Pelo JW, Worthington MT, Sturgill TW. MAPKAP kinase 2 phosphorylates tris-tetraprolin on in vivo sites including Ser178, a site required for 14-3-3 binding. J Biol Chem. 2004;279:10176-10184.
21. Manke IA, Nguyen A, Lim D, Stewart MQ, Elia AE, Yaffe MB. MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation. Mol Cell. 2005;17:37-48.
22. Stoecklin G, Stubbs T, Kedersha N, Wax S, Rigby WF, Blackwell TK, Anderson P. MK2-induced tristetraprolin:14 -3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J. 2004;23: 1313-1324.
23. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M. Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphoryla-tion of the small mammalian heat shock proteins. FEBS Lett. 1992;313: 307-313.
24. Wang X, Khaleque MA, Zhao MJ, Zhong R, Gaestel M, Calderwood SK. Phosphorylation of HSF1 by MAPK-activated protein kinase 2 on serine 121, inhibits transcriptional activity and promotes HSP90 binding. J Biol Chem. 2006;281:782-791.
25. Zheng C, Lin Z, Zhao ZJ, Yang Y, Niu H, Shen X. MAPK-activated protein kinase-2 (MK2)-mediated formation and phosphorylation-regulated dissociation of the signal complex consisting of p38, MK2, Akt, and Hsp27. J Biol Chem. 2006;281:37215-37226.
26. Ronkina N, Kotlyarov A, Dittrich-Breiholz O, Kracht M, Hitti E, Milarski K, Askew R, Marusic S, Lin LL, Gaestel M, Telliez JB. The mitogen-activated protein kinase (MAPK)-activated protein kinases MK2 and MK3 cooperate in stimulation of tumor necrosis factor biosynthesis and stabilization of p38 MAPK. Mol Cell Biol. 2007;27:170-181.
27. Kotlyarov A, Yannoni Y, Fritz S, Laass K, Telliez JB, Pitman D, Lin LL, Gaestel M. Distinct cellular functions of MK2. Mol Cell Biol. 2002;22: 4827-4835.
28. Touyz RM, Tolloczko B, Schiffrin EL. Mesenteric vascular smooth muscle cells from spontaneously hypertensive rats display increased calcium responses to angiotensin II but not to endothelin-1. J Hypertens. 1994;12:663-673.
29. Rey FE, Cifuentes ME, Kiarash A, Quinn MT, Pagano PJ. Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ Res. 2001;89:408-414.
30. Morin S, Paradis P, Aries A, Nemer M. Serum response factor-GATA ternary complex required for nuclear signaling by a G-protein-coupled receptor. Mol Cell Biol. 2001;21:1036-1044.
31. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-386.
32. Li L, Fink GD, Watts SW, Northcott CA, Galligan JJ, Pagano PJ, Chen AF. Endothelin-1 increases vascular superoxide via endothelin(A)-NADPH oxidase pathway in low-renin hypertension. Circulation. 2003;107: 1053-1058.
33. Touyz RM, Yao G, Viel E, Amiri F, Schiffrin EL. Angiotensin II and endothelin-1 regulate MAP kinases through different redox-dependent mechanisms in human vascular smooth muscle cells. J Hypertens. 2004; 22:1141-1149.
34. Bunkenburg B, van AT, Rogg H, Wood JM. Receptor-mediated effects of angiotensin II on growth of vascular smooth muscle cells from spontaneously hypertensive rats. Hypertension. 1992;20:746-754.
35. Behr TM, Nerurkar SS, Nelson AH, Coatney RW, Woods TN, Sulpizio A, Chandra S, Brooks DP, Kumar S, Lee JC, Ohlstein EH, Angermann CE, Adams JL, Sisko J, Sackner-Bernstein JD, Willette RN. Hypertensive end-organ damage and premature mortality are p38 mitogen-activated protein kinase-dependent in a rat model of cardiac hypertrophy and dysfunction. Circulation. 2001;104:1292-1298.
36. Widder J, Behr T, Fraccarollo D, Hu K, Galuppo P, Tas P, Angermann CE, Ertl G, Bauersachs J. Vascular endothelial dysfunction and superoxide anion production in heart failure are p38 MAP kinase-dependent. Cardiovasc Res. 2004;63:161-167.
37. Sugden PH, Clerk A. "Stress-responsive" mitogen-activated protein kinases (c-Jun N-terminal kinases and p38 mitogen-activated protein kinases) in the myocardium. Circ Res. 1998;83:345-352.
38. Bao W, Behm DJ, Nerurkar SS, Ao Z, Bentley R, Mirabile RC, Johns DG, Woods TN, Doe CP, Coatney RW, Ohlstein JF, Douglas SA, Willette RN, Yue TL. Effects of p38 MAPK Inhibitor on angiotensin II-dependent hypertension, organ damage, and superoxide anion production. J Cardiovasc Pharmacol. 2007;49:362-368.
39. Hippenstiel S, Soeth S, Kellas B, Fuhrmann O, Seybold J, Krull M, Eichel-Streiber C, Goebeler M, Ludwig S, Suttorp N. Rho proteins and the p38-MAPK pathway are important mediators for LPS-induced interleukin-8 expression in human endothelial cells. Blood. 2000;95: 3044-3051.
40. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, McNulty D, Blumenthal MJ, Heys JR, Landvatter SW. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature. 1994;372:739-746.
41. Takahashi M, Suzuki E, Takeda R, Oba S, Nishimatsu H, Kimura K, Nagano T, Nagai R, Hirata Y. Angiotensin II and tumor necrosis factor-alpha synergistically promote monocyte chemoattractant protein-1 expression: roles of NF-kappaB, p38, and reactive oxygen species. Am J Physiol Heart Circ Physiol. 2008;294:H2879-H2888.
42. Wang Y, Zeigler MM, Lam GK, Hunter MG, Eubank TD, Khramtsov VV, Tridandapani S, Sen CK, Marsh CB. The role of the NADPH oxidase complex, p38 MAPK, and Akt in regulating human monocyte/macro-phage survival. Am J Respir Cell Mol Biol. 2007;36:68-77.
43. Zhan Y, Brown C, Maynard E, Anshelevich A, Ni W, Ho IC, Oettgen P. Ets-1 is a critical regulator of Ang II-mediated vascular inflammation and remodeling. J Clin Invest. 2005;115:2508-2516.
44. Taniyama Y, Hitomi H, Shah A, Alexander RW, Griendling KK. Mechanisms of reactive oxygen species-dependent downregulation of insulin receptor substrate-1 by angiotensin II. Arterioscler Thromb Vasc Biol. 2005;25:1142-1147.
45. Viedt C, Soto U, Krieger-Brauer HI, Fei J, Elsing C, Kubler W, Kreuzer J. Differential activation of mitogen-activated protein kinases in smooth muscle cells by angiotensin II: involvement of p22phox and reactive oxygen species. Arterioscler Thromb Vasc Biol. 2000;20:940-948.
46. Touyz RM, Chen X, Tabet F, Yao G, He G, Quinn MT, Pagano PJ, Schiffrin EL. Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ Res. 2002;90: 1205-1213.
47. Ni W, Zhan Y, He H, Maynard E, Balschi JA, Oettgen P. Ets-1 is a critical transcriptional regulator of reactive oxygen species and p47(phox) gene expression in response to angiotensin II. Circ Res. 2007;101: 985-994.
48. Jeney V, Itoh S, Wendt M, Gradek Q, Ushio-Fukai M, Harrison DG, Fukai T. Role of antioxidant-1 in extracellular superoxide dismutase function and expression. Circ Res. 2005;96:723-729.
49. Zhou X, Bohlen HG, Miller SJ, Unthank JL. NAD(P)H oxidase-derived peroxide mediates elevated basal and impaired flow-induced NO production in SHR mesenteric arteries in vivo. Am J Physiol Heart Circ Physiol. 2008;295:H1008-H1016.
50. Bagi Z, Erdei N, Koller A. High intraluminal pressure via H2O2 upregulates arteriolar constrictions to angiotensin II by increasing the functional availability of AT1 receptors. Am J Physiol Heart Circ Physiol. 2008;295:H835-H841.
51. Zhang Y, Griendling KK, Dikalova A, Owens GK, Taylor WR. Vascular hypertrophy in angiotensin II-induced hypertension is mediated by vascular smooth muscle cell-derived H2O2. Hypertension. 2005;46: 732-737. (Pubitemid 43186746)
52. Touyz RM, He G, El MM, Diep Q, Mardigyan V, Schiffrin EL. Differential activation of extracellular signal-regulated protein kinase 1/2 and p38 mitogen activated-protein kinase by AT1 receptors in vascular smooth muscle cells from Wistar-Kyoto rats and spontaneously hypertensive rats. J Hypertens. 2001;19:553-559.
53. Chen S, Qiong Y, Gardner DG. A role for p38 mitogen-activated protein kinase and c-myc in endothelin-dependent rat aortic smooth muscle cell proliferation. Hypertension. 2006;47:252-258.
54. Streicher JM, Ren S, Herschman H, Wang Y. MAPK-activated protein kinase-2 in cardiac hypertrophy and cyclooxygenase-2 regulation in heart. Circ Res. 2010;106:1434-1443.