Published online before print September 8, 2005, doi: 10.1161/01.RES.0000185804.79157.C0
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Submitted on April 18, 2005
Revised on August 28, 2005
Accepted on August 30, 2005
NADPH Oxidase-Derived Superoxide Anion Mediates Angiotensin II-Induced Pressor Effect via Activation of p38 Mitogen-Activated Protein Kinase in the Rostral Ventrolateral Medulla
Samuel H.H. Chan ;
From the Center for Neuroscience, National Sun Yat-sen University (S.H.H.C.), Kaohsiung; Department of Pharmacology, National Cheng Kung University (K.S.H., C.C.H.), Tainan; and Department of Medical Education and Research, Kaohsiung Veterans General Hospital (L.L.W., C.C.O., J.Y.H.C.), Kaohsiung, Taiwan, Republic of China.
* To whom correspondence should be addressed. E-mail: yhwa{at}isca.vghks.gov.tw.
The rostral ventrolateral medulla (RVLM), where sympathetic premotor neurons are located, is a central site via which angiotensin II (Ang II) elicits its pressor effect. We tested the hypothesis that NADPH oxidase-derived superoxide anion (O2·-) in the RVLM mediates Ang II-induced pressor response via activation of mitogen-activated protein kinase (MAPK) signaling pathways. Bilateral microinjection of Ang II into the RVLM resulted in an angiotensin subtype 1 (AT1) receptor-dependent phosphorylation of p38 MAPK and extracellular signal-regulated protein kinase (ERK)1/2, but not stress-activated protein kinase/Jun N-terminal kinase (SAPK/JNK), in the ventrolateral medulla. The Ang II-induced p38 MAPK or ERK1/2 phosphorylation was attenuated by application into the RVLM of a NADPH oxidase inhibitor, diphenyleneiodonium chloride (DPI), an antisense oligonucleotide that targets against p22phox or p47phox subunit of NADPH oxidase mRNA, or the superoxide dismutase mimetic tempol. DPI or antisense p22phox or p47phox oligonucleotide treatment also attenuated the AT1 receptor-dependent increase in O2·- production in the ventrolateral medulla elicited by Ang II at the RVLM. Functionally, Ang II-elicited pressor response in the RVLM was attenuated by DPI, tempol, or a p38 MAPK inhibitor, SB203580. The AT1 receptor-mediated enhancement of the frequency of glutamate-sensitive spontaneous excitatory postsynaptic currents induced by Ang II in RVLM neurons was also abolished by SB203580. These results suggest that NADPH oxidase-derived O2·- underlies the activation of p38 MAPK or ERK1/2 by Ang II in the ventrolateral medulla. Furthermore, the p38 MAPK signaling pathway may mediate Ang II-induced pressor response via enhancement of presynaptic release of glutamate to RVLM neurons.
Key words: mitogen-activated protein kinases • angiotensin II • superoxide anion • NADPH oxidase • rostral ventrolateral medulla • blood pressure
Related Article:
- The Regulation of Sympathetic Nerve Activity by Angiotensin II Involves Reactive Oxygen Species and MAPK
- Irving H. Zucker and Lie Gao
Circ. Res. 2005 97: 737-739.[Extract] [Full Text] [PDF]
This article has been cited by other articles:
 |
|
 |
|
  I. H. Zucker, H. D. Schultz, K. P. Patel, W. Wang, and L. Gao Regulation of central angiotensin type 1 receptors and sympathetic outflow in heart failure Am J Physiol Heart Circ Physiol, November 1, 2009; 297(5): H1557 - H1566. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. R. Peterson, M. A. Burmeister, X. Tian, Y. Zhou, M. R. Guruju, J. A. Stupinski, R. V. Sharma, and R. L. Davisson Genetic Silencing of Nox2 and Nox4 Reveals Differential Roles of These NADPH Oxidase Homologues in the Vasopressor and Dipsogenic Effects of Brain Angiotensin II Hypertension, November 1, 2009; 54(5): 1106 - 1114. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. H.H. Chan, C.-A. Wu, K. L.H. Wu, Y.-H. Ho, A. Y.W. Chang, and J. Y.H. Chan Transcriptional Upregulation of Mitochondrial Uncoupling Protein 2 Protects Against Oxidative Stress-Associated Neurogenic Hypertension Circ. Res., October 23, 2009; 105(9): 886 - 896. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Israel, J. Arzola, S. De Jesus, and M. Varela Role of oxidative stress in the natriuresis induced by central administration of angiotensin II Journal of Renin-Angiotensin-Aldosterone System, March 1, 2009; 10(1): 9 - 14. [Abstract] [PDF]
|
|
|
|
|
|
S. H.H. Chan, K. L.H. Wu, A. Y.W. Chang, M.-H. Tai, and J. Y.H. Chan Oxidative Impairment of Mitochondrial Electron Transport Chain Complexes in Rostral Ventrolateral Medulla Contributes to Neurogenic Hypertension Hypertension, February 1, 2009; 53(2): 217 - 227. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. S. Wilcox and A. Pearlman Chemistry and Antihypertensive Effects of Tempol and Other Nitroxides Pharmacol. Rev., December 1, 2008; 60(4): 418 - 469. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L.-C. Kung, S. H. H. Chan, K. L. H. Wu, C.-C. Ou, M.-H. Tai, and J. Y. H. Chan Mitochondrial Respiratory Enzyme Complexes in Rostral Ventrolateral Medulla as Cellular Targets of Nitric Oxide and Superoxide Interaction in the Antagonism of Antihypertensive Action of eNOS Transgene Mol. Pharmacol., November 1, 2008; 74(5): 1319 - 1332. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Wang, T. A. Milner, R. C. Speth, A. C. Gore, D. Wu, C. Iadecola, and J. P. Pierce Sex differences in angiotensin signaling in bulbospinal neurons in the rat rostral ventrolateral medulla Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2008; 295(4): R1149 - R1157. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Gao, W.-Z. Wang, W. Wang, and I. H. Zucker Imbalance of Angiotensin Type 1 Receptor and Angiotensin II Type 2 Receptor in the Rostral Ventrolateral Medulla: Potential Mechanism for Sympathetic Overactivity in Heart Failure Hypertension, October 1, 2008; 52(4): 708 - 714. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-G. Wei, Y. Yu, Z.-H. Zhang, R. M. Weiss, and R. B. Felder Angiotensin II-Triggered p44/42 Mitogen-Activated Protein Kinase Mediates Sympathetic Excitation in Heart Failure Rats Hypertension, August 1, 2008; 52(2): 342 - 350. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Liu, L. Gao, S. K. Roy, K. G. Cornish, and I. H. Zucker Role of Oxidant Stress on AT1 Receptor Expression in Neurons of Rabbits With Heart Failure and in Cultured Neurons Circ. Res., July 18, 2008; 103(2): 186 - 193. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Nagaoka, L. Kuo, Y. Ren, A. Yoshida, and T. W. Hein C-Reactive Protein Inhibits Endothelium-Dependent Nitric Oxide-Mediated Dilation of Retinal Arterioles via Enhanced Superoxide Production Invest. Ophthalmol. Vis. Sci., May 1, 2008; 49(5): 2053 - 2060. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Kvochina, E. M. Hasser, and C. M. Heesch Pregnancy increases baroreflex-independent GABAergic inhibition of the RVLM in rats Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2007; 293(6): R2295 - R2305. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G.-X. Zhang, X.-M. Lu, S. Kimura, and A. Nishiyama Role of mitochondria in angiotensin II-induced reactive oxygen species and mitogen-activated protein kinase activation Cardiovasc Res, November 1, 2007; 76(2): 204 - 212. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Fujita, K. Ando, A. Nagae, and T. Fujita Sympathoexcitation by Oxidative Stress in the Brain Mediates Arterial Pressure Elevation in Salt-Sensitive Hypertension Hypertension, August 1, 2007; 50(2): 360 - 367. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Belardinelli Exercise Training in Chronic Heart Failure: How to Harmonize Oxidative Stress, Sympathetic Outflow, and Angiotensin II Circulation, June 19, 2007; 115(24): 3042 - 3044. [Full Text] [PDF]
|
|
|
|
 |
|
 Q. Chen and H.-L. Pan Signaling Mechanisms of Angiotensin II-Induced Attenuation of GABAergic Input to Hypothalamic Presympathetic Neurons J Neurophysiol, May 1, 2007; 97(5): 3279 - 3287. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. N. Mayorov Brain superoxide as a key regulator of the cardiovascular response to emotional stress in rabbits Exp Physiol, May 1, 2007; 92(3): 471 - 479. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-K. Park, R. Fischer, R. Dechend, E. Shagdarsuren, A. Gapeljuk, M. Wellner, S. Meiners, P. Gratze, N. Al-Saadi, S. Feldt, et al. p38 Mitogen-Activated Protein Kinase Inhibition Ameliorates Angiotensin II-Induced Target Organ Damage Hypertension, March 1, 2007; 49(3): 481 - 489. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Y. H. Chan, H.-L. Cheng, J. L. J. Chou, F. C. H. Li, K.-Y. Dai, S. H. H. Chan, and A. Y. W. Chang Heat Shock Protein 60 or 70 Activates Nitric-oxide Synthase (NOS) I- and Inhibits NOS II-associated Signaling and Depresses the Mitochondrial Apoptotic Cascade during Brain Stem Death J. Biol. Chem., February 16, 2007; 282(7): 4585 - 4600. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. W. Weiss, M. D. Y. Liu, and J. Huang Sleep Apnoea & Hypertension: Physiological bases for a causal relation: Physiological basis for a causal relationship of obstructive sleep apnoea to hypertension Exp Physiol, January 1, 2007; 92(1): 21 - 26. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. H. Zucker Novel Mechanisms of Sympathetic Regulation in Chronic Heart Failure Hypertension, December 1, 2006; 48(6): 1005 - 1011. [Full Text] [PDF]
|
|
|
|
 |
|
 Y.-J. Peng, G. Yuan, F. J. Jacono, G. K. Kumar, and N. R. Prabhakar 5-HT evokes sensory long-term facilitation of rodent carotid body via activation of NADPH oxidase J. Physiol., October 1, 2006; 576(1): 289 - 295. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Y. W. Chang, J. Y. H. Chan, J. L. J. Chou, F. C. H. Li, K.-Y. Dai, and S. H. H. Chan Heat shock protein 60 in rostral ventrolateral medulla reduces cardiovascular fatality during endotoxaemia in the rat J. Physiol., July 15, 2006; 574(2): 547 - 564. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Zhou, C. Ziegler, L. A. Birder, A. F.R. Stewart, and E. S. Levitan Angiotensin II and Stretch Activate NADPH Oxidase to Destabilize Cardiac Kv4.3 Channel mRNA Circ. Res., April 28, 2006; 98(8): 1040 - 1047. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. H. Zucker and L. Gao The Regulation of Sympathetic Nerve Activity by Angiotensin II Involves Reactive Oxygen Species and MAPK Circ. Res., October 14, 2005; 97(8): 737 - 739. [Full Text] [PDF]
|
|