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Efferent Vagal Fibre Stimulation Blunts Nuclear Factor-κB Activation and Protects Against Hypovolemic Hemorrhagic Shock
Open accessAbstract
Background— We investigated whether electrical stimulation (STIM) of efferent vagus nerves may suppress nuclear factor (NF)-κB activation and the inflammatory cascade in hemorrhagic (Hem) shock. Methods and Results— Rats were subjected to bilateral cervical vagotomy (VGX) or sham surgical procedures. Hem shock was induced by intermittent withdrawing of blood until mean arterial pressure stabilized within the range of 35 to 40 mm Hg. Application of constant voltage pulses to the caudal vagus ends (STIM; 5 V, 2 ms, 1 Hz for 12 minutes, 5 minutes after mean arterial pressure stabilization) increased survival time (VGX+Hem+Sham STIM=38±3 minutes; VGX+Hem+STIM >180 minutes), reverted the marked hypotension (VGX+Hem+Sham STIM=33±3 mm Hg; VGX+Hem+STIM=66±5 mm Hg), inhibited IκBα liver loss, and blunted the augmented NF-κB activity, decreased hepatic tumor necrosis factor (TNF)-α mRNA (VGX+Hem+Sham STIM=1.42±0.5 amount of TNF-α m-RNA; VGX+Hem+STIM=0.51±0.2 amount of TNF-α mRNA), and reduced plasma TNF-α (VGX+Hem+Sham STIM=190±24 pg/mL; VGX+Hem+STIM=87±15 pg/mL). Chlorisondamine, a nicotinic receptor antagonist, abated the effects of vagal stimulation. Conclusions— Our results show a parasympathetic inhibition of NF-κB by which the brain opposes NF-κB activation in the liver and modulates the inflammatory response during acute hypovolemic hemorrhagic shock.
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“The protective effects of vagus nerve stimulation in this model were reversed by administration of a nicotine receptor antagonist (chlorisondamine), indicating that vagus nerve control of cytokine damage is attributable to cholinergic signals transduced intracellularly via nicotinic receptors (21).”
From Physiology and immunology of the cholinergic antiinflammatory pathway (2007) · cites this paper as [21]
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“Vagus nerve stimulation of rats during lethal hemorrhagic shock conferred significant protection against the development of hypotension, prolonged survival, and decreased TNF production (21).”
From Physiology and immunology of the cholinergic antiinflammatory pathway (2007) · cites this paper as [21]
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“As occurs in circulatory shock, HS024 and chlorisondamine - at a dose able to block central MC4 and peripheral nicotinic receptors, respectively (Guarini et al., 2003; 2004; Altavilla et al., 2006; Giuliani et al., 2007) - counteracted the effect of NDP-a-MSH on the mRNA expression of TNF-a and…”
BackgroundMethodInfluentialSelf-citationMravec, B., Gidron, Y., Kukanova, B., Bízik, J., Kiss, A., & Hulín, I. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.07.003 · Cited by 26
The contribution of the nervous system in the cancer progression
Park, H., & Lee, C. H. (2024) · BMB Reports · doi:10.5483/bmbrep.2024-0019 · Cited by 25
“Acetylcholine secreted by T-ChAT cells subsequently elicit anti-inflammatory effect by inhibiting the nuclear translocation of nuclear factor κ B (nuclear factor κ B) and activation of JAK2-STAT3 pathway through the α 7-nicoti-nic acetylcholine receptor ( α 7nAChR) expressed in macrophages (67-69).”
BackgroundAnesthesia-specific protection from endotoxic shock is not mediated through the vagus nerve
Fuentes, J. M., Hanly, E. J., Aurora, A. R., Maio, A. D., & Talamini, M. A. (2005) · Surgery · doi:10.1016/j.surg.2005.06.057 · Cited by 25
“Other studies have shown that efferent vagal signals inhibit nuclear factor-jB during acute hypovolemic shock.(12) Thus communication through the vagus nerve between the central nervous system and the periphery is bidirectional with respect to maintenance of equilibrium during stress and inflammation.”
BackgroundEffect of Acute Traumatic Brain Injury on Baroreflex Function
McMahon, C. G., Kenny, R. A., Bennett, K., Little, R. A., & Kirkman, E. (2010) · Shock · doi:10.1097/shk.0b013e3181e687c6 · Cited by 24
Minutoli, L., Squadrito, F., Nicòtina, P. A., Giuliani, D., Ottani, A., Polito, F., Bitto, A., Irrera, N., Guzzo, G., Spaccapelo, L., et al. (2011) · Critical Care Medicine · doi:10.1097/ccm.0b013e318207ea80 · Cited by 24
“On the other hand, cervical vagotomy, as well as pretreatment with the nicotinic acetylcholine receptor antagonist chlorisondamine (at a dose able to block only peripheral receptors) (14, 26) and the selective melanocortin MC4 receptor antagonist HS024 (19, 30), abated the protective effects of RO273225 (Fig.”
BackgroundMethodSelf-citationRetractedSánchez‐Alemán, E., Quintanar‐Stephano, A., Escobedo, G., Campos-Esparza, M. D. R., Campos‐Rodríguez, R., & Ventura‐Juárez, J. (2014) · NeuroImmunoModulation · doi:10.1159/000362240 · Cited by 23
Freeling, J., Wattier, K., LaCroix, C., & Li, Y. (2007) · Experimental Physiology · doi:10.1113/expphysiol.2007.039784 · Cited by 23
“In animal studies, stimulation of cholinergic vagal nerves induced significant anti-inflammatory effects by inhibiting the expression of TNFα, IL-1α and IL-6 in systemic inflammatory states (Borovikova et al. 2000; Guarini et al. 2003; Wang et al. 2003).”
BackgroundAbdullahi, A., Wong, T. W. L., & Ng, S. S. M. (2023) · Cancer Medicine · doi:10.1002/cam4.6466 · Cited by 22
Tanaka, S., HAMMOND, B. F., Rosin, D. L., & Okusa, M. D. (2019) · Bioelectronic Medicine · doi:10.1186/s42234-019-0029-8 · Cited by 22
Long-Term Follow-Up of Solitary Intracerebral Juvenile Xanthogranuloma
Fulkerson, D. H., Luerssen, T. G., Hattab, E. M., et al. (2008) · Pediatric Neurosurgery · doi:10.1159/000180303 · Cited by 21
Clinical approach to autonomic dysfunction
Wells, R. M., & Tonkin, A. (2016) · Internal Medicine Journal · doi:10.1111/imj.13216 · Cited by 20
Yang, L., & Dong, X. (2017) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2016.0137 · Cited by 20
Protective effects of the melanocortin analog NDP-α-MSH in rats undergoing cardiac arrest
Ottani, A., Neri, L., Canalini, F., Calevro, A., Rossi, R., Cappelli, G., Ballestri, M., Giuliani, D., & Guarini, S. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.10.022 · Cited by 19
“The arterial catheter was connected to a pressure transducer coupled to a Surveyor apparatus (Mortara-Rangoni, Bologna, Italy), as previously described (Guarini et al., 1996, 1997a, 1997b, 2003).”
BackgroundMethodSelf-citationInhibition of acute lung inflammation by a neuroimmune circuit induced by vagal nerve stimulation
Murray, K. M., Cremin, M., Tay, E. X. Y., Sanchez, K., Schreiber, S., Lloyd, E., Brust‐Mascher, I., Leigh, W. A., Ashfaq, J., Gareau, M. G., et al. (2025) · Science Advances · doi:10.1126/sciadv.adw7080 · Cited by 24
“T cell–derived ACh activates nicotinic alpha 7 receptors ( α 7R) on macrophages, blocking nuclear factor κ B signaling and transcription of pro-inflammatory cytokines such as tumor necrosis factor– α (TNF α ) ( 17 – 19 ).”
Collateral benefits of studying the vagus nerve in bioelectronic medicine
Pavlov, V. A. (2019) · Bioelectronic Medicine · doi:10.1186/s42234-019-0021-3 · Cited by 19
Li, M., Zheng, C., Kawada, T., Inagaki, M., Uemura, K., Akiyama, T., & Sugimachi, M. (2020) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-020-07062-1 · Cited by 19
Kashihara, K., Kawada, T., Li, M., et al. (2004) · The Japanese Journal of Physiology · doi:10.2170/jjphysiol.54.395 · Cited by 19
Sitapara, R. A., Gauthier, A. G., Patel, V., Lin, M., Zur, M., Ashby, C. R., & Mantell, L. L. (2020) · Molecular Medicine · doi:10.1186/s10020-020-00224-9 · Cited by 19
Effects of Nicotine and Vagus Nerve in Severe Acute Pancreatitis–Associated Lung Injury in Rats
Ma, P., Yu, K., Yu, J., Wang, W., Ding, Y., Chen, C., Chen, X., Zhao, K., Zuo, T., He, X., et al. (2015) · Pancreas · doi:10.1097/mpa.0000000000000575 · Cited by 18
LOW‐DOSE PROPOFOL AMELIORATES HAEMORRHAGIC SHOCK‐INDUCED ORGAN DAMAGE IN CONSCIOUS RATS
Lee, C., Subeq, Y., Lee, R., Wu, W., & Hsu, B. (2008) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2007.04859.x · Cited by 18
“Efferent activity in the vagus nerve can prevent HS by inhibiting nuclear factor (NF)-kB and attenuating TNF-a synthesis, and its effect is dependent on nicotinic a-bungarotoxin-sensitive acetylcholine receptors on macrophages.(34) The cholinergic anti-inflammatory pathway has also been reported to be involved in sept…”
BackgroundOptogenetic stimulation of the brainstem dorsal motor nucleus ameliorates acute pancreatitis
Thompson, D., Tsaava, T., Rishi, A., Nadella, S., Mishra, L., Tuveson, D. A., Pavlov, V. A., Brines, M. L., Tracey, K. J., & Chavan, S. S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1166212 · Cited by 18
Xia, H., Liu, Z., Liang, W., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/1079129 · Cited by 17
H2S and Oxytocin Systems in Early Life Stress and Cardiovascular Disease
McCook, O., Denoix, N., Radermacher, P., Waller, C., & Merz, T. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10163484 · Cited by 16
Veiz, E., Kieslich, S.-K., Czesnik, D., Herrmann‐Lingen, C., Meyer, T., & Staab, J. (2022) · NeuroImmunoModulation · doi:10.1159/000524646 · Cited by 16
Ottani, A., Giuliani, D., Neri, L., Calevro, A., Canalini, F., Vandini, E., Cainazzo, M. M., Ruberto, A. I., Barbieri, A., Rossi, R., et al. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.10.022 · Cited by 17
Self-citationHigh-fat nutrition reduces hepatic damage following exposure to bacterial DNA and hemorrhagic shock
Luyer, M. D. P., Derikx, J. P. M., Beyaert, R., Hadfoune, M., Kuppevelt, T. H. V., Dejong, C. H. C., Heineman, E., Buurman, W. A., & Greve, J. W. M. (2008) · Journal of Hepatology · doi:10.1016/j.jhep.2008.08.025 · Cited by 17
“Stimulation of this anti-inflammatory pathway is known to reduce the release of inflammatory mediators in a variety of experimental models including hemorrhagic shock, ileus and peritonitis [13,28,29].”
BackgroundZhou, L., Lin, X., Ma, X., Liu, Y., Ma, L., Chen, Z., Chen, H., Si, L., & Chen, X. (2020) · International Journal of Neuroscience · doi:10.1080/00207454.2019.1706504 · Cited by 16
Zhao, Y., Sun, H., Li, K., Shang, L., Liang, X., Yang, H., Dong, Z., Xiaokereti, J., Shang, S., Zhou, Q., et al. (2021) · Mediators of Inflammation · doi:10.1155/2021/4504431 · Cited by 15
Metadata
- Authors
- Guarini, S., Altavilla, D., Cainazzo, M.-M., Giuliani, D., Bigiani, A., Marini, H., Squadrito, G., Minutoli, L., Bertolini, A., Marini, R., Adamo, E. B., Venuti, F. S., & Squadrito, F.
- Affiliations
- University of Modena and Reggio Emilia (IT)
- ORCID
- Venue
- Circulation
- Published
- 2003-03-04
- Volume
- 107
- Issue
- 8
- Pages
- 1189-1194
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- OpenAlex
- W2098655301
- Semantic Scholar
- 919d8a5ae0075ccd6d7dd152a6fe9773763923b4
- Cited by
- 315
- References
- 24
- Citations by year
- 2026: 2 · 2025: 10 · 2024: 9 · 2023: 8 · 2022: 14 · 2021: 13 · 2020: 18 · 2019: 12 · 2018: 10 · 2017: 15 · 2016: 10 · 2015: 18 · 2014: 22 · 2013: 16 · 2012: 21
- FWCI
- 6.64
- Type
- journal article
- Language
- en
- Update notices
- expression_of_concern (2022-08-23)
- Open access
- green
- hdl.handle.net
- Licence
- cc-by
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
- Funders
- Consiglio Nazionale delle Ricerche
- Università degli Studi di Messina
- Topics
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Trauma, Hemostasis, Coagulopathy, Resuscitation
- Keywords
- vagus nerve stimulation, NF-κB activation, inflammation, TNF-α, parasympathetic nervous system, vagotomy, nicotinic acetylcholine receptors, liver inflammation
- MeSH terms
- NF-KappaB Inhibitor alpha, Animals, Blood Pressure, Efferent Pathways, Electric Stimulation, Inflammation, Liver, Male, Nerve Fibers, RNA, Messenger, Shock, Hemorrhagic, Tumor Necrosis Factor-alpha, Vagus Nerve, Survival Analysis, NF-kappa B, Rats, Wistar, I-kappa B Proteins, Hypovolemia, Rats
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