Cited by 271Nitric Oxide and Endothelin EffectsHeart Rate Variability and Autonomic ControlBlood Pressure and Hypertension Studies

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A central nervous system action of nitric oxide in blood pressure regulation

Togashi, H, Sakuma, I, Yoshioka, M, Kobayashi, T, Yasuda, H, Kitabatake, A, Saito, H, Gross, S S, Levi, R·1992·The Journal of Pharmacology and Experimental Therapeutics

DOI 10.1016/s0022-3565(25)10757-x

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Abstract

We had reported that the systemic administration of N omega-methyl-L-arginine (L-NMA), a specific inhibitor of nitric oxide (NO) synthesis from L-arginine (ARG), raises arterial blood pressure (BP) while paradoxically enhancing central sympathetic outflow. Cervical spinal cord transection abolishes the increase in sympathetic outflow and attenuates the pressor effect of L-NMA. Thus, in addition to lowering BP by direct vasorelaxation, NO may also act in the central nervous system to reduce vascular sympathetic tone. To test this hypothesis we have injected L-NMA directly into the central nervous system in anesthetized rats. Intracisternally (i.c.), L-NMA elicited a small pressor response accompanied by a marked increase in sympathetic renal nerve activity (RNA). In contrast, the inactive stereoisomer N omega-methyl-D-arginine had neither pressor nor neural effects. The increases in RNA and BP elicited by i.c. L-NMA were abolished by spinal cord transection at C1 to C2 and by the i.v. administration of ARG. When administered i.c., ARG also abolished the increase in RNA elicited by i.v. L-NMA and significantly attenuated the pressor response. Thus, our findings indicate that L-NMA acts centrally by an ARG-reversible mechanism in the anesthetized rat to stimulate sympathetic nerve activity. Inasmuch as centrally synthesized NO has been postulated to play a second messenger and/or neurotransmitter role, our findings suggest that one such function would be the central regulation of sympathetic outflow and hence, BP.

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Mills, P. C., Marlin, D., SCOTT, C. M., & Smith, N. C. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.82.4.1035 · Cited by 45
“NO has been shown to dilate cutaneous vasculature (4, 7) while inhibitors of NO synthase (NOS; the enzyme responsible for NO production), such as NGnitro-L-arginine methyl ester (L-NAME), have been shown to cross the blood-brain barrier (25) and exert a pressor response (6, 12), probably by enhancing central sympathet…”
Background
Role of nitric oxide synthase inhibition in the acute hypertensive response to intracerebroventricular cadmium
Demontis, M. P., Varoni, M. V., Volpe, A. R., et al. (1998) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0701573 · Cited by 45
“Availability of L-Arg could be a rate-limiting factor for NO biosynthesis in tissues that were deprived of substrate or during administration of substrate analogues (Hecker et al, 1990; Togashi et al., 1992; Tseng et al., 1996).”
BackgroundMethod
l -NAME- and ADMA-induced sympathetic neural activation in conscious rats
Augustyniak, R. A., Victor, R. G., Morgan, D. A., & Zhang, W. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00768.2004 · Cited by 44
“First, previous findings in anesthetized animals, which demonstrated that NOS inhibitors administered either centrally (9, 48, 50) or via intravenous infusion in sino-aortic-denervated animals (7, 10, 26, 29, 41) caused an increase in SNA above the baseline level of neural firing, can now be extrapolated to the consci…”
Role of nitric oxide in the nucleus of the solitary tract of rats
Matsumura, K., Tsuchihashi, T., Kagiyama, S., et al. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00420-x · Cited by 43
Nitric oxide is an excitatory modulator in the rostral ventrolateral medulla in rats
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Influence of Carbon Monoxide, and its Interaction with Nitric Oxide, on the Adrenocorticotropin Hormone Response of the Normal Rat to a Physico‐Emotional Stress
Turnbull, A. V., Kim, C. K., Lee, S., et al. (1998) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1998.00266.x · Cited by 42
Effects of Angiotensin II on NO Bioavailability Evaluated Using a Catheter-Type NO Sensor
Imanishi, T., Kobayashi, K., Kuroi, A., Mochizuki, S., Goto, M., Yoshida, K., & Akasaka, T. (2006) · Hypertension · doi:10.1161/01.hyp.0000248920.16956.d8 · Cited by 41
Blunted nitric oxide-mediated inhibition of sympathetic nerve activity within the paraventricular nucleus in diabetic rats
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“Using perforated patchclamp recording, Li et al. (17) found GABAergic synaptic activity in the PVN neurons was potentiated by NO donors, and the NO-mediated inhibition of firing activity was blocked by the GABA receptor antagonist.”
BackgroundInfluential
Ramipril prevents the detrimental sequels of chronic NO synthase inhibition in rats: hypertension, cardiac hypertrophy and renal insufficiency
Hropot, M., Gr�tsch, H., Klaus, E., Langer, K. H., Linz, W., Wiemer, G., & lkens, B. A. S. (1994) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00169370 · Cited by 41
“Since ACE inhib i t ion a t tenuated L-NAME-induced hypertension, it seems that angio tens in II is involved in the mechan i sm of this type of hypertension, a l though the involvement of neural mechanisms can not be excluded (Togashi et al. 1992; Toda et al. 1993).”
Background
Central and Peripheral Effects of Asymmetric Dimethylarginine, an Endogenous Nitric Oxide Synthetase Inhibitor
Jin, J., & D’Alecy, L. G. (1996) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199609000-00014 · Cited by 41
Role of Renal Nerves in Mediating the Hypertensive Effects of Nitric Oxide Synthesis Inhibition
Granger, J. P., Novak, J., Schnackenberg, C. G., Williams, S., & Reinhart, G. A. (1996) · Hypertension · doi:10.1161/01.hyp.27.3.613 · Cited by 40
Microinfusion of a Nitric Oxide Donor in Discrete Brain Regions Activates the Hypothalamic‐Pituitary‐Adrenal Axis
Seo, D. O., & RIVIER, C. L. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00690.x · Cited by 36
Nitric oxide reduces blood pressure in the nucleus tractus solitarius: a real time electrochemical study
Wu, W. C., Wang, Y., Kao, L. S., Tang, F., & Chai, C. Y. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00737-7 · Cited by 38

Authors: Togashi, H., Sakuma, I., Yoshioka, M., Kobayashi, T., Yasuda, H., Kitabatake, A., Saito, H., Gross, S. S., & Levi, R.
Affiliations: Hokkaido University (JP)
ORCID: Sakuma, I
Kobayashi, T
Saito, H
Levi, R
Venue: The Journal of Pharmacology and Experimental Therapeutics
Publisher: Elsevier BV
Published: 1992-07
Volume: 262
Issue: 1
Pages: 343-347
ISSN: 0022-3565 (ISSN-L)
DOI: 10.1016/s0022-3565(25)10757-x
OpenAlex: W1953075977
Cited by: 270
References: 0
Citations by year: 2022: 3 · 2021: 6 · 2020: 2 · 2019: 4 · 2017: 3 · 2016: 2 · 2015: 5 · 2014: 4 · 2013: 8 · 2012: 5
FWCI: 10.61
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Journal of Pharmacology and Experimental Therapeutics (publishedVersion)
PubMed (publishedVersion)
PubMed
Funders: National Heart, Lung, and Blood Institute (P01HL046403, HL-46403, HL-34215, R01HL034215)
Topics: Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Blood Pressure and Hypertension Studies
Keywords: nitric oxide, blood pressure regulation, L-arginine, central nervous system, sympathetic activity, renal sympathetic nerve activity, pressor response, spinal cord transection, intracisternal administration, neurotransmitter function, vasorelaxation
MeSH terms: Animals, Arginine, Blood Pressure, Central Nervous System, Heart Rate, Male, Nitric Oxide, Pressoreceptors, Rats, Inbred Strains, RNA, omega-N-Methylarginine, Rats

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A central nervous system action of nitric oxide in blood pressure regulation

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