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(Circulation Research. 1995;77:29-36.)
© 1995 American Heart Association, Inc.

Articles

Differential Activation of Mitogen-Activated Protein Kinases by H₂O₂ and O₂^- in Vascular Smooth Muscle Cells

Arnold S. Baas, Bradford C. Berk

From the Cardiology Division, Department of Internal Medicine, University of Washington, Seattle.

Correspondence to Bradford C. Berk, MD, PhD, Cardiology Division, RG-22, University of Washington, Seattle, WA 98195. E-mail bcberk@u.washington.edu.

Abstract Increased generation of active oxygen species such as H₂O₂ and O₂^- may be important in vascular smooth muscle cell growth associated with atherosclerosis and restenosis. In previous work, we showed that H₂O₂ stimulated vascular smooth muscle cell growth and proto-oncogene expression. In the present study, we compared the effects of H₂O₂ and O₂^- on cultured rat aortic vascular smooth muscle cell growth and signal transduction. O₂^- was generated in a concentration-dependent manner by the naphthoquinolinedione LY83583. Vascular smooth muscle cell growth, as measured by [³H]thymidine incorporation, was stimulated by 200 µmol/L H₂O₂ (110% increase versus 0.1% serum) and 1 µmol/L LY83583 (175% increase) to levels comparable to 10 ng/mL platelet-derived growth factor (210% increase). Since activation of mitogen-activated protein kinase (MAP kinase) is one of the earliest growth factor signal events, the activity of MAP kinase was measured by changes in mobility on Western blot and by phosphorylation of myelin basic protein. There was a concentration-dependent increase in MAP kinase activity by LY83583 (maximum, 10 µmol/L) but not by H₂O₂. The time course for activation of MAP kinase by LY83583 showed a maximum at 5 to 10 minutes with return to baseline by 20 minutes. Activation of MAP kinase by LY83583 was protein kinase C dependent. Expression of MAP kinase phosphatase-1 (MKP-1), a transcriptionally regulated redox-sensitive protein tyrosine/threonine phosphatase, was also measured. Although H₂O₂ induced MKP-1 mRNA to a greater extent than did LY83583, the increased MKP-1 expression could not explain the inability of H₂O₂ to stimulate MAP kinase, because mRNA levels were not detected until 60 minutes. The findings that both O₂^- and H₂O₂ stimulate vascular smooth muscle cell growth but only O₂^- rapidly activates MAP kinase suggest that additional signal events are required for the mitogenic effects of H₂O₂.

Key Words: mitogen-activated protein kinase • signal transduction • H₂O₂ • O₂^- • mitogen-activated protein kinase phosphatase-1

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				J.-i. Abe and B. C. Berk Fyn and JAK2 Mediate Ras Activation by Reactive Oxygen Species J. Biol. Chem., July 23, 1999; 274(30): 21003 - 21010. [Abstract] [Full Text] [PDF]

				T. E. Peterson, V. Poppa, H. Ueba, A. Wu, C. Yan, and B. C. Berk Opposing Effects of Reactive Oxygen Species and Cholesterol on Endothelial Nitric Oxide Synthase and Endothelial Cell Caveolae Circ. Res., July 9, 1999; 85(1): 29 - 37. [Abstract] [Full Text] [PDF]

				L.-H. Yeh, Y. J. Park, R. J. Hansalia, I. S. Ahmed, S. S. Deshpande, P. J. Goldschmidt-Clermont, K. Irani, and B. R. Alevriadou Shear-induced tyrosine phosphorylation in endothelial cells requires Rac1-dependent production of ROS Am J Physiol Cell Physiol, April 1, 1999; 276(4): C838 - C847. [Abstract] [Full Text] [PDF]

				G. N. Rao, K. A. Katki, N. R. Madamanchi, Y. Wu, and M. J. Birrer JunB Forms the Majority of the AP-1 Complex and Is a Target for Redox Regulation by Receptor Tyrosine Kinase and G Protein-coupled Receptor Agonists in Smooth Muscle Cells J. Biol. Chem., February 26, 1999; 274(9): 6003 - 6010. [Abstract] [Full Text] [PDF]

				R. Zent, M. Ailenberg, G. P. Downey, and M. Silverman ROS stimulate reorganization of mesangial cell-collagen gels by tyrosine kinase signaling Am J Physiol Renal Physiol, February 1, 1999; 276(2): F278 - F287. [Abstract] [Full Text] [PDF]

				B. Metzler, Y. Hu, G. Sturm, G. Wick, and Q. Xu Induction of Mitogen-activated Protein Kinase Phosphatase-1 by Arachidonic Acid in Vascular Smooth Muscle Cells J. Biol. Chem., December 11, 1998; 273(50): 33320 - 33326. [Abstract] [Full Text] [PDF]

				D. Wang, X. Yu, and P. Brecher Nitric Oxide and N-Acetylcysteine Inhibit the Activation of Mitogen-activated Protein Kinases by Angiotensin II in Rat Cardiac Fibroblasts J. Biol. Chem., December 4, 1998; 273(49): 33027 - 33034. [Abstract] [Full Text] [PDF]

				G. Lu, E. L. Greene, T. Nagai, and B. M. Egan Reactive Oxygen Species Are Critical in the Oleic Acid–Mediated Mitogenic Signaling Pathway in Vascular Smooth Muscle Cells Hypertension, December 1, 1998; 32(6): 1003 - 1010. [Abstract] [Full Text] [PDF]

				T. Goldkorn, N. Balaban, K. Matsukuma, V. Chea, R. Gould, J. Last, C. Chan, and C. Chavez EGF-Receptor Phosphorylation and Signaling Are Targeted by H2O2 Redox Stress Am. J. Respir. Cell Mol. Biol., November 1, 1998; 19(5): 786 - 798. [Abstract] [Full Text]

				A. M. Zafari, M. Ushio-Fukai, M. Akers, Q. Yin, A. Shah, D. G. Harrison, W. R. Taylor, and K. K. Griendling Role of NADH/NADPH Oxidase–Derived H2O2 in Angiotensin II–Induced Vascular Hypertrophy Hypertension, September 1, 1998; 32(3): 488 - 495. [Abstract] [Full Text] [PDF]

				J. Zhang, N. Jin, Y. Liu, and R. A. Rhoades Hydrogen Peroxide Stimulates Extracellular Signal-regulated Protein Kinases in Pulmonary Arterial Smooth Muscle Cells Am. J. Respir. Cell Mol. Biol., August 1, 1998; 19(2): 324 - 332. [Abstract] [Full Text]

				M. Ushio-Fukai, R. W. Alexander, M. Akers, and K. K. Griendling 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., June 12, 1998; 273(24): 15022 - 15029. [Abstract] [Full Text] [PDF]

				A. Sabri, K. L. Byron, A. M. Samarel, J. Bell, and P. A. Lucchesi Hydrogen Peroxide Activates Mitogen-Activated Protein Kinases and Na+-H+ Exchange in Neonatal Rat Cardiac Myocytes Circ. Res., June 1, 1998; 82(10): 1053 - 1062. [Abstract] [Full Text] [PDF]

				G. W. De Keulenaer, D. C. Chappell, N. Ishizaka, R. M. Nerem, R. W. Alexander, and K. K. Griendling Oscillatory and Steady Laminar Shear Stress Differentially Affect Human Endothelial Redox State : Role of a Superoxide-Producing NADH Oxidase Circ. Res., June 1, 1998; 82(10): 1094 - 1101. [Abstract] [Full Text] [PDF]

				M. K. Abe, S. Kartha, A. Y. Karpova, J. Li, P. T. Liu, W.-L. Kuo, and M. B. Hershenson Hydrogen Peroxide Activates Extracellular Signal-regulated Kinase via Protein Kinase C, Raf-1, and MEK1 Am. J. Respir. Cell Mol. Biol., April 1, 1998; 18(4): 562 - 569. [Abstract] [Full Text]

				A. Clerk, S. J. Fuller, A. Michael, and P. H. Sugden Stimulation of "Stress-regulated" Mitogen-activated Protein Kinases (Stress-activated Protein Kinases/c-Jun N-terminal Kinases and p38-Mitogen-activated Protein Kinases) in Perfused Rat Hearts by Oxidative and Other Stresses J. Biol. Chem., March 27, 1998; 273(13): 7228 - 7234. [Abstract] [Full Text] [PDF]

				J. Ruef, G. N. Rao, F. Li, C. Bode, C. Patterson, A. Bhatnagar, and M. S. Runge Induction of Rat Aortic Smooth Muscle Cell Growth by the Lipid Peroxidation Product 4-Hydroxy-2-Nonenal Circulation, March 24, 1998; 97(11): 1071 - 1078. [Abstract] [Full Text] [PDF]

				J. M. Pyles, K. L. March, M. Franklin, K. Mehdi, R. L. Wilensky, and L. P. Adam Activation of MAP Kinase In Vivo Follows Balloon Overstretch Injury of Porcine Coronary and Carotid Arteries Circ. Res., December 19, 1997; 81(6): 904 - 910. [Abstract] [Full Text]

				P.-F. Li, R. Dietz, and R. von Harsdorf Differential Effect of Hydrogen Peroxide and Superoxide Anion on Apoptosis and Proliferation of Vascular Smooth Muscle Cells Circulation, November 18, 1997; 96(10): 3602 - 3609. [Abstract] [Full Text]

				T. Marumo, V. B. Schini-Kerth, B. Fisslthaler, and R. Busse Platelet-Derived Growth Factor–Stimulated Superoxide Anion Production Modulates Activation of Transcription Factor NF-{kappa}B and Expression of Monocyte Chemoattractant Protein 1 in Human Aortic Smooth Muscle Cells Circulation, October 7, 1997; 96(7): 2361 - 2367. [Abstract] [Full Text]

				J.-i. Abe, M. Takahashi, M. Ishida, J.-D. Lee, and B. C. Berk c-Src Is Required for Oxidative Stress-mediated Activation of Big Mitogen-activated Protein Kinase 1 (BMK1) J. Biol. Chem., August 15, 1997; 272(33): 20389 - 20394. [Abstract] [Full Text] [PDF]