Understanding the Pivotal Role of the Vagus Nerve in Health from Pandemics
Abstract
:1. Introduction: Searching for a Single Anti-Infectious Solution
2. Invasion of the Vagus Nerve by Pathogens Appears as a Common Key Step in Host Defense in the Last Two Pandemics
3. The Vagus Nerve Seems Essential to Neuroimmunometabolism and Health
4. Discussion: Novel Therapies Targeting Vagus Nerve Stimulation for Pandemics
5. Conclusions: The Pivotal Role of the Vagus Nerve, beyond Pandemics
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Izda, V.; Jeffries, M.A.; Sawalha, A.H. COVID-19: A Review of Therapeutic Strategies and Vaccine Candidates. Clin. Immunol. 2021, 222, 108634. [Google Scholar] [CrossRef] [PubMed]
- Priyadarsini, S.L.; Suresh, M.; Huisingh, D. What Can We Learn from Previous Pandemics to Reduce the Frequency of Emerging Infectious Diseases like COVID-19? Glob. Transit. 2020, 2, 202–220. [Google Scholar] [CrossRef] [PubMed]
- Lopes Fischer, N.; Naseer, N.; Shin, S.; Brodsky, I.E. Effector-Triggered Immunity and Pathogen Sensing in Metazoans. Nat. Microbiol. 2020, 5, 14–26. [Google Scholar] [CrossRef] [PubMed]
- Hoffman, C.; Aballay, A. Role of Neurons in the Control of Immune Defense. Curr. Opin. Immunol. 2019, 60, 30–36. [Google Scholar] [CrossRef] [PubMed]
- Pavlov, V.A.; Tracey, K.J. The Vagus Nerve and the Inflammatory Reflex—Linking Immunity and Metabolism. Nat. Rev. Endocrinol. 2012, 8, 743–754. [Google Scholar] [CrossRef] [PubMed]
- Rosas-Ballina, M.; Tracey, K.J. Cholinergic Control of Inflammation. J. Intern. Med. 2009, 265, 663–679. [Google Scholar] [CrossRef]
- Azzaz, F.; Yahi, N.; Di Scala, C.; Chahinian, H.; Fantini, J. Ganglioside Binding Domains in Proteins: Physiological and Pathological Mechanisms. In Advances in Protein Chemistry and Structural Biology; Elsevier: Amsterdam, The Netherlands, 2022; Volume 128, pp. 289–324. ISBN 978-0-323-98895-7. [Google Scholar]
- Duerr, R.; Crosse, K.M.; Valero-Jimenez, A.M.; Dittmann, M. SARS-CoV-2 Portrayed against HIV: Contrary Viral Strategies in Similar Disguise. Microorganisms 2021, 9, 1389. [Google Scholar] [CrossRef]
- Changeux, J.-P.; Amoura, Z.; Rey, F.A.; Miyara, M. A Nicotinic Hypothesis for COVID-19 with Preventive and Therapeutic Implications. C. R. Biol. 2020, 343, 33–39. [Google Scholar] [CrossRef]
- Lagoumintzis, G.; Chasapis, C.T.; Alexandris, N.; Kouretas, D.; Tzartos, S.; Eliopoulos, E.; Farsalinos, K.; Poulas, K. Nicotinic Cholinergic System and COVID-19: In Silico Identification of Interactions between A7 Nicotinic Acetylcholine Receptor and the Cryptic Epitopes of SARS-Co-V and SARS-CoV-2 Spike Glycoproteins. Food Chem. Toxicol. 2021, 149, 112009. [Google Scholar] [CrossRef] [PubMed]
- Farsalinos, K.; Eliopoulos, E.; Leonidas, D.D.; Papadopoulos, G.E.; Tzartos, S.; Poulas, K. Nicotinic Cholinergic System and COVID-19: In Silico Identification of an Interaction between SARS-CoV-2 and Nicotinic Receptors with Potential Therapeutic Targeting Implications. Int. J. Mol. Sci. 2020, 21, 5807. [Google Scholar] [CrossRef] [PubMed]
- Kopańska, M.; Batoryna, M.; Bartman, P.; Szczygielski, J.; Banaś-Ząbczyk, A. Disorders of the Cholinergic System in COVID-19 Era—A Review of the Latest Research. Int. J. Mol. Sci. 2022, 23, 672. [Google Scholar] [CrossRef] [PubMed]
- Bracci, L.; Lozzi, L.; Rustici, M.; Neri, P. Binding of HIV-1 Gp120 to the Nicotinic Receptor. FEBS Lett. 1992, 311, 115–118. [Google Scholar] [CrossRef] [Green Version]
- Iturriaga-Vásquez, P.; Alzate-Morales, J.; Bermudez, I.; Varas, R.; Reyes-Parada, M. Multiple Binding Sites in the Nicotinic Acetylcholine Receptors: An Opportunity for Polypharmacolgy. Pharmacol. Res. 2015, 101, 9–17. [Google Scholar] [CrossRef] [PubMed]
- Gundavarapu, S.; Mishra, N.C.; Singh, S.P.; Langley, R.J.; Saeed, A.I.; Feghali-Bostwick, C.A.; McIntosh, J.M.; Hutt, J.; Hegde, R.; Buch, S.; et al. HIV Gp120 Induces Mucus Formation in Human Bronchial Epithelial Cells through CXCR4/A7-Nicotinic Acetylcholine Receptors. PLoS ONE 2013, 8, e77160. [Google Scholar] [CrossRef]
- Capó-Vélez, C.M.; Morales-Vargas, B.; García-González, A.; Grajales-Reyes, J.G.; Delgado-Vélez, M.; Madera, B.; Báez-Pagán, C.A.; Quesada, O.; Lasalde-Dominicci, J.A. The Alpha7-Nicotinic Receptor Contributes to Gp120-Induced Neurotoxicity: Implications in HIV-Associated Neurocognitive Disorders. Sci. Rep. 2018, 8, 1829. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, T.; Gong, Z.; Wan, Y.; Li, Y.; Gao, X.; Lun, J.; Huang, S.; Cao, H. Establishment of a gp120 transgenic mouse model with α7 nAChR knockout. Nan Fang Yi Ke Da Xue Xue Bao 2020, 40, 1184–1191. [Google Scholar] [CrossRef] [PubMed]
- Zoli, M.; Pucci, S.; Vilella, A.; Gotti, C. Neuronal and Extraneuronal Nicotinic Acetylcholine Receptors. Curr. Neuropharmacol. 2018, 16, 338–349. [Google Scholar] [CrossRef]
- Mao, D.; Yasuda, R.P.; Fan, H.; Wolfe, B.B.; Kellar, K.J. Heterogeneity of Nicotinic Cholinergic Receptors in Rat Superior Cervical and Nodose Ganglia. Mol. Pharmacol. 2006, 70, 1693–1699. [Google Scholar] [CrossRef]
- Wang, J.; Meng, J.; Nugent, M.; Tang, M.; Dolly, J.O. Neuronal Entry and High Neurotoxicity of Botulinum Neurotoxin A Require Its N-Terminal Binding Sub-Domain. Sci. Rep. 2017, 7, 44474. [Google Scholar] [CrossRef] [Green Version]
- Rangon, C.-M.; Krantic, S.; Moyse, E.; Fougère, B. The Vagal Autonomic Pathway of COVID-19 at the Crossroad of Alzheimer’s Disease and Aging: A Review of Knowledge. J. Alzheimers Dis. Rep. 2020, 4, 537–551. [Google Scholar] [CrossRef] [PubMed]
- Bulfamante, G.; Bocci, T.; Falleni, M.; Campiglio, L.; Coppola, S.; Tosi, D.; Chiumello, D.; Priori, A. Brainstem Neuropathology in Two Cases of COVID-19: SARS-CoV-2 Trafficking between Brain and Lung. J. Neurol. 2021, 268, 4486–4491. [Google Scholar] [CrossRef] [PubMed]
- Gentile, F.; Bocci, T.; Coppola, S.; Pozzi, T.; Modafferi, L.; Priori, A.; Chiumello, D. Putative Role of the Lung–Brain Axis in the Pathogenesis of COVID-19-Associated Respiratory Failure: A Systematic Review. Biomedicines 2022, 10, 729. [Google Scholar] [CrossRef] [PubMed]
- Ríos, S.C.; Colón Sáez, J.O.; Quesada, O.; Figueroa, K.Q.; Lasalde Dominicci, J.A. Disruption of the Cholinergic Anti-Inflammatory Response by R5-Tropic HIV-1 Protein Gp120JRFL. J. Biol. Chem. 2021, 296, 100618. [Google Scholar] [CrossRef] [PubMed]
- Goodman, B.P.; Khoury, J.A.; Blair, J.E.; Grill, M.F. COVID-19 Dysautonomia. Front. Neurol. 2021, 12, 624968. [Google Scholar] [CrossRef] [PubMed]
- Robinson-Papp, J.; Nmashie, A.; Pedowitz, E.; Benn, E.K.T.; George, M.C.; Sharma, S.; Murray, J.; Machac, J.; Heiba, S.; Mehandru, S.; et al. Vagal Dysfunction and Small Intestinal Bacterial Overgrowth: Novel Pathways to Chronic Inflammation in HIV. AIDS 2018, 32, 1147–1156. [Google Scholar] [CrossRef]
- Robinson-Papp, J.; Sharma, S.K. Autonomic Neuropathy in HIV Is Unrecognized and Associated with Medical Morbidity. AIDS Patient Care STDs 2013, 27, 539–543. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Al-Harthi, L.; Campbell, E.; Schneider, J.A.; Bennett, D.A. What HIV in the Brain Can Teach Us About SARS-CoV-2 Neurological Complications? AIDS Res. Hum. Retrovir. 2021, 37, 255–265. [Google Scholar] [CrossRef]
- Woods, S.P.; Moore, D.J.; Weber, E.; Grant, I. Cognitive Neuropsychology of HIV-Associated Neurocognitive Disorders. Neuropsychol. Rev. 2009, 19, 152–168. [Google Scholar] [CrossRef] [Green Version]
- Braak, H.; Rüb, U.; Gai, W.P.; Del Tredici, K. Idiopathic Parkinson’s Disease: Possible Routes by Which Vulnerable Neuronal Types May Be Subject to Neuroinvasion by an Unknown Pathogen. J. Neural Transm. 2003, 110, 517–536. [Google Scholar] [CrossRef]
- Petrakis, S.; Irinopoulou, T.; Panagiotidis, C.H.; Engelstein, R.; Lindstrom, J.; Orr-Urtreger, A.; Gabizon, R.; Grigoriadis, N.; Sklaviadis, T. Cellular Prion Protein Co-Localizes with NAChR Β4 Subunit in Brain and Gastrointestinal Tract. Eur. J. Neurosci. 2008, 27, 612–620. [Google Scholar] [CrossRef]
- Kresl, P.; Rahimi, J.; Gelpi, E.; Aldecoa, I.; Ricken, G.; Danics, K.; Keller, E.; Kovacs, G.G. Accumulation of Prion Protein in the Vagus Nerve in Creutzfeldt–Jakob Disease. Ann. Neurol. 2019, 85, 782–787. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mol, M.B.A.; Strous, M.T.A.; van Osch, F.H.M.; Vogelaar, F.J.; Barten, D.G.; Farchi, M.; Foudraine, N.A.; Gidron, Y. Heart-Rate-Variability (HRV), Predicts Outcomes in COVID-19. PLoS ONE 2021, 16, e0258841. [Google Scholar] [CrossRef] [PubMed]
- Pan, Y.; Yu, Z.; Yuan, Y.; Han, J.; Wang, Z.; Chen, H.; Wang, S.; Wang, Z.; Hu, H.; Zhou, L.; et al. Alteration of Autonomic Nervous System Is Associated With Severity and Outcomes in Patients With COVID-19. Front. Physiol. 2021, 12, 630038. [Google Scholar] [CrossRef]
- Leitzke, M.; Stefanovic, D.; Meyer, J.-J.; Schimpf, S.; Schönknecht, P. Autonomic Balance Determines the Severity of COVID-19 Courses. Bioelectron. Med. 2020, 6, 22. [Google Scholar] [CrossRef] [PubMed]
- Gonçalves, A.J.; Braga, M.V.A.; Santana, P.H.; Resende, L.A.P.R.; da Silva, V.J.D.; Correia, D. Linear and Non-Linear Analysis of Heart Rate Variability in HIV-Positive Patients on Two Different Antiretroviral Therapy Regimens. BMC Infect. Dis. 2021, 21, 1022. [Google Scholar] [CrossRef] [PubMed]
- Scherzer, R.; Shah, S.J.; Secemsky, E.; Butler, J.; Grunfeld, C.; Shlipak, M.G.; Hsue, P.Y. Association of Biomarker Clusters With Cardiac Phenotypes and Mortality in Patients With HIV Infection. Circ. Heart Fail. 2018, 11, e004312. [Google Scholar] [CrossRef] [PubMed]
- Fairchild, K.D.; Srinivasan, V.; Randall Moorman, J.; Gaykema, R.P.A.; Goehler, L.E. Pathogen-Induced Heart Rate Changes Associated with Cholinergic Nervous System Activation. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 2011, 300, R330–R339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Molinero, M.; Benítez, I.D.; González, J.; Gort-Paniello, C.; Moncusí-Moix, A.; Rodríguez-Jara, F.; García-Hidalgo, M.C.; Torres, G.; Vengoechea, J.J.; Gómez, S.; et al. Bronchial Aspirate-Based Profiling Identifies MicroRNA Signatures Associated With COVID-19 and Fatal Disease in Critically Ill Patients. Front. Med. 2022, 8, 756517. [Google Scholar] [CrossRef]
- Sabbatinelli, J.; Giuliani, A.; Matacchione, G.; Latini, S.; Laprovitera, N.; Pomponio, G.; Ferrarini, A.; Svegliati Baroni, S.; Pavani, M.; Moretti, M.; et al. Decreased Serum Levels of the Inflammaging Marker MiR-146a Are Associated with Clinical Non-Response to Tocilizumab in COVID-19 Patients. Mech. Ageing Dev. 2021, 193, 111413. [Google Scholar] [CrossRef]
- Visacri, M.B.; Nicoletti, A.S.; Pincinato, E.C.; Loren, P.; Saavedra, N.; Saavedra, K.; Salazar, L.A.; Moriel, P. Role of MiRNAs as Biomarkers of COVID-19: A Scoping Review of the Status and Future Directions for Research in This Field. Biomark. Med. 2021, 15, 1785–1795. [Google Scholar] [CrossRef]
- Tang, H.; Gao, Y.; Li, Z.; Miao, Y.; Huang, Z.; Liu, X.; Xie, L.; Li, H.; Wen, W.; Zheng, Y.; et al. The Noncoding and Coding Transcriptional Landscape of the Peripheral Immune Response in Patients with COVID-19. Clin. Transl. Med. 2020, 10, e200. [Google Scholar] [CrossRef] [PubMed]
- Leo, C.G.; Mincarone, P.; Tumolo, M.R.; Panico, A.; Guido, M.; Zizza, A.; Guarino, R.; De Santis, G.; Sedile, R.; Sabina, S. MiRNA Expression Profiling in HIV Pathogenesis, Disease Progression and Response to Treatment: A Systematic Review. Epigenomics 2021, 13, 1653–1671. [Google Scholar] [CrossRef]
- Reynoso, R.; Laufer, N.; Hackl, M.; Skalicky, S.; Monteforte, R.; Turk, G.; Carobene, M.; Quarleri, J.; Cahn, P.; Werner, R.; et al. MicroRNAs Differentially Present in the Plasma of HIV Elite Controllers Reduce HIV Infection in Vitro. Sci. Rep. 2015, 4, 5915. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pogue, A.I.; Lukiw, W.J. MicroRNA-146a-5p, Neurotropic Viral Infection and Prion Disease (PrD). Int. J. Mol. Sci. 2021, 22, 9198. [Google Scholar] [CrossRef] [PubMed]
- Brenneman, D.E.; McCune, S.K.; Mervis, R.F.; Hill’, J.M. Gp120 as an Etiologic Agent for NeuroAIDS: Neurotoxicity and Model Systems. Adv. Neuroimmunol. 1994, 4, 157–165. [Google Scholar] [CrossRef]
- Mitra, S.; Banik, A.; Saurabh, S.; Maulik, M.; Khatri, S.N. Neuroimmunometabolism: A New Pathological Nexus Underlying Neurodegenerative Disorders. J. Neurosci. 2022, 42, 1888–1907. [Google Scholar] [CrossRef]
- Berthoud, H.; Neuhuber, W.L. Vagal Mechanisms as Neuromodulatory Targets for the Treatment of Metabolic Disease. Ann. N. Y. Acad. Sci. 2019, 1454, 42–55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cotero, V.; Miwa, H.; Graf, J.; Ashe, J.; Loghin, E.; Di Carlo, D.; Puleo, C. Peripheral Focused Ultrasound Neuromodulation (PFUS). J. Neurosci. Methods 2020, 341, 108721. [Google Scholar] [CrossRef]
- Fülling, C.; Dinan, T.G.; Cryan, J.F. Gut Microbe to Brain Signaling: What Happens in Vagus. Neuron 2019, 101, 998–1002. [Google Scholar] [CrossRef] [Green Version]
- Wachsmuth, H.R.; Weninger, S.N.; Duca, F.A. Role of the Gut–Brain Axis in Energy and Glucose Metabolism. Exp. Mol. Med. 2022, 54, 377–392. [Google Scholar] [CrossRef]
- Ludwig, M.Q.; Cheng, W.; Gordian, D.; Lee, J.; Paulsen, S.J.; Hansen, S.N.; Egerod, K.L.; Barkholt, P.; Rhodes, C.J.; Secher, A.; et al. A Genetic Map of the Mouse Dorsal Vagal Complex and Its Role in Obesity. Nat. Metab. 2021, 3, 530–545. [Google Scholar] [CrossRef] [PubMed]
- Bonaz, B.; Sinniger, V.; Pellissier, S. Anti-Inflammatory Properties of the Vagus Nerve: Potential Therapeutic Implications of Vagus Nerve Stimulation: Anti-Inflammatory Effect of Vagus Nerve Stimulation. J. Physiol. 2016, 594, 5781–5790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Falvey, A.; Metz, C.N.; Tracey, K.J.; Pavlov, V.A. Peripheral Nerve Stimulation and Immunity: The Expanding Opportunities for Providing Mechanistic Insight and Therapeutic Intervention. Int. Immunol. 2022, 34, 107–118. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; George, S.J.; Thompson, D.A.; Silverman, H.A.; Tsaava, T.; Tynan, A.; Pavlov, V.A.; Chang, E.H.; Andersson, U.; Brines, M.; et al. Famotidine Activates the Vagus Nerve Inflammatory Reflex to Attenuate Cytokine Storm. Mol. Med. 2022, 28, 57. [Google Scholar] [CrossRef] [PubMed]
- Calder, P.C. Nutrition, Immunity and COVID-19. BMJ Nutr. Prev. Health 2020, 3, 74–92. [Google Scholar] [CrossRef] [PubMed]
- Serhan, C.N.; Rosa, X.; Jouvene, C. Novel Mediators and Mechanisms in the Resolution of Infectious Inflammation: Evidence for Vagus Regulation. J. Intern. Med. 2019, 286, 240–258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Watanabe, H.; Shima, S.; Mizutani, Y.; Ueda, A.; Ito, M. Long COVID: Pathogenesis and Therapeutic Approach. Brain Nerve Shinkei Kenkyu No Shinpo 2022, 74, 879–884. [Google Scholar] [CrossRef]
- Palmer, C.S.; Cherry, C.L.; Sada-Ovalle, I.; Singh, A.; Crowe, S.M. Glucose Metabolism in T Cells and Monocytes: New Perspectives in HIV Pathogenesis. EBioMedicine 2016, 6, 31–41. [Google Scholar] [CrossRef] [Green Version]
- Kang, S.; Tang, H. HIV-1 Infection and Glucose Metabolism Reprogramming of T Cells: Another Approach Toward Functional Cure and Reservoir Eradication. Front. Immunol. 2020, 11, 572677. [Google Scholar] [CrossRef]
- Das, U.N. Obesity: Genes, Brain, Gut, and Environment. Nutrition 2010, 26, 459–473. [Google Scholar] [CrossRef]
- Lu, J.; Piper, S.J.; Zhao, P.; Miller, L.J.; Wootten, D.; Sexton, P.M. Targeting VIP and PACAP Receptor Signaling: New Insights into Designing Drugs for the PACAP Subfamily of Receptors. Int. J. Mol. Sci. 2022, 23, 8069. [Google Scholar] [CrossRef]
- Yasui, A.; Naruse, S.; Yanaihara, C.; Ozaki, T.; Hoshino, M.; Mochizuki, T.; Daniel, E.E.; Yanaihara, N. Corelease of PHI and VIP by Vagal Stimulation in the Dog. Am. J. Physiol.-Gastrointest. Liver Physiol. 1987, 253, G13–G19. [Google Scholar] [CrossRef] [PubMed]
- Lundberg, J.M.; Hökfelt, T.; Kewenter, J.; Pettersson, G.; Ahlman, H.; Edin, R.; Dahlström, A.; Nilsson, G.; Terenius, L.; Uvnäs-Wallensten, K.; et al. Substance P-, VIP-, and Enkephalin-like Immunoreactivity in the Human Vagus Nerve. Gastroenterology 1979, 77, 468–471. [Google Scholar] [CrossRef]
- Lundberg, J.M.; Änggärd, A.; Fahrenkrug, J.; Hökfelt, T.; Mutt, V. Vasoactive Intestinal Polypeptide in Cholinergic Neurons of Exocrine Glands: Functional Significance of Coexisting Transmitters for Vasodilation and Secretion. Proc. Natl. Acad. Sci. USA 1980, 77, 1651–1655. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Magistretti, P.J.; Cardinaux, J.-R.; Martin, J.-L. VIP and PACAP in the CNS: Regulators of Glial Energy Metabolism and Modulators of Glutamatergic Signalinga. Ann. N. Y. Acad. Sci. 1998, 865, 213–225. [Google Scholar] [CrossRef]
- Matsushita, N.; Kato, Y.; Shimatsu, A.; Katakami, H.; Yanaihara, N.; Imura, H. Effects of VIP, TRH, GABA and Dopamine on Prolactin Release from Superfused Rat Anterior Pituitary Cells. Life Sci. 1983, 32, 1263–1269. [Google Scholar] [CrossRef]
- Malhotra, R.K.; Wakade, A.R. Vasoactive Intestinal Polypeptide Stimulates the Secretion of Catecholamines from the Rat Adrenal Gland. J. Physiol. 1987, 388, 285–294. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ganea, D. Regulatory Effects of Vasoactive Intestinal Peptide on Cytokine Production in Central and Peripheral Lymphoid Organs. Adv. Neuroimmunol. 1996, 6, 61–74. [Google Scholar] [CrossRef]
- Sanders, T.H.; Weiss, J.; Hogewood, L.; Chen, L.; Paton, C.; McMahan, R.L.; Sweatt, J.D. Cognition-Enhancing Vagus Nerve Stimulation Alters the Epigenetic Landscape. J. Neurosci. 2019, 39, 3454–3469. [Google Scholar] [CrossRef] [Green Version]
- Zhong, X.; Liao, Y.; Chen, L.; Liu, G.; Feng, Y.; Zeng, T.; Zhang, J. The MicroRNAs in the Pathogenesis of Metabolic Memory. Endocrinology 2015, 156, 3157–3168. [Google Scholar] [CrossRef]
- Cao, Y.; Pan, S.; Yan, M.; Sun, C.; Huang, J.; Zhong, C.; Wang, L.; Yi, L. Flexible and Stretchable Polymer Optical Fibers for Chronic Brain and Vagus Nerve Optogenetic Stimulations in Free-Behaving Animals. BMC Biol. 2021, 19, 252. [Google Scholar] [CrossRef]
- Murray, K.; Rude, K.M.; Sladek, J.; Reardon, C. Divergence of Neuroimmune Circuits Activated by Afferent and Efferent Vagal Nerve Stimulation in the Regulation of Inflammation. J. Physiol. 2021, 599, 2075–2084. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, U.; Chang, Y.-C.; Zafeiropoulos, S.; Nassrallah, Z.; Miller, L.; Zanos, S. Strategies for Precision Vagus Neuromodulation. Bioelectron. Med. 2022, 8, 9. [Google Scholar] [CrossRef] [PubMed]
- Lancaster, K.Z.; Pfeiffer, J.K. Limited Trafficking of a Neurotropic Virus through Inefficient Retrograde Axonal Transport and the Type I Interferon Response. PLoS Pathog. 2010, 6, e1000791. [Google Scholar] [CrossRef] [PubMed]
- Johnson, R.L.; Wilson, C.G. A Review of Vagus Nerve Stimulation as a Therapeutic Intervention. J. Inflamm. Res. 2018, 11, 203–213. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pomfrett, C.J.D.; Glover, D.G.; Pollard, B.J. The Vagus Nerve as a Conduit for Neuroinvasion, a Diagnostic Tool, and a Therapeutic Pathway for Transmissible Spongiform Encephalopathies, Including Variant Creutzfeld Jacob Disease. Med. Hypotheses 2007, 68, 1252–1257. [Google Scholar] [CrossRef]
- Nicholson, W.C.; Kempf, M.-C.; Moneyham, L.; Vance, D.E. The Potential Role of Vagus-Nerve Stimulation in the Treatment of HIV-Associated Depression: A Review of Literature. Neuropsychiatr. Dis. Treat. 2017, 13, 1677–1689. [Google Scholar] [CrossRef] [Green Version]
- Guo, Z.-P.; Sörös, P.; Zhang, Z.-Q.; Yang, M.-H.; Liao, D.; Liu, C.-H. Use of Transcutaneous Auricular Vagus Nerve Stimulation as an Adjuvant Therapy for the Depressive Symptoms of COVID-19: A Literature Review. Front. Psychiatry 2021, 12, 765106. [Google Scholar] [CrossRef] [PubMed]
- Rangon, C.-M.; Barruet, R.; Mazouni, A.; Le Cossec, C.; Thevenin, S.; Guillaume, J.; Léguillier, T.; Huysman, F.; Luis, D. Auricular Neuromodulation for Mass Vagus Nerve Stimulation: Insights From SOS COVID-19 a Multicentric, Randomized, Controlled, Double-Blind French Pilot Study. Front. Physiol. 2021, 12, 704599. [Google Scholar] [CrossRef] [PubMed]
- Tornero, C.; Pastor, E.; del Garzando, M.M.; Orduña, J.; Forner, M.J.; Bocigas, I.; Cedeño, D.L.; Vallejo, R.; McClure, C.K.; Czura, C.J.; et al. Non-Invasive Vagus Nerve Stimulation for COVID-19: Results From a Randomized Controlled Trial (SAVIOR I). Front. Neurol. 2022, 13, 820864. [Google Scholar] [CrossRef]
- Seitz, T.; Szeles, J.C.; Kitzberger, R.; Holbik, J.; Grieb, A.; Wolf, H.; Akyaman, H.; Lucny, F.; Tychera, A.; Neuhold, S.; et al. Percutaneous Auricular Vagus Nerve Stimulation Reduces Inflammation in Critical COVID-19 Patients. Front. Physiol. 2022, 13, 897257. [Google Scholar] [CrossRef]
- Go, Y.-Y.; Ju, W.-M.; Lee, C.-M.; Chae, S.-W.; Song, J.-J. Different Transcutaneous Auricular Vagus Nerve Stimulation Parameters Modulate the Anti-Inflammatory Effects on Lipopolysaccharide-Induced Acute Inflammation in Mice. Biomedicines 2022, 10, 247. [Google Scholar] [CrossRef]
- Courties, A.; Boussier, J.; Hadjadj, J.; Yatim, N.; Barnabei, L.; Péré, H.; Veyer, D.; Kernéis, S.; Carlier, N.; Pène, F.; et al. Regulation of the Acetylcholine/A7nAChR Anti-Inflammatory Pathway in COVID-19 Patients. Sci. Rep. 2021, 11, 11886. [Google Scholar] [CrossRef] [PubMed]
- Czura, C.J.; Bikson, M.; Charvet, L.; Chen, J.D.Z.; Franke, M.; Fudim, M.; Grigsby, E.; Hamner, S.; Huston, J.M.; Khodaparast, N.; et al. Neuromodulation Strategies to Reduce Inflammation and Improve Lung Complications in COVID-19 Patients. Front. Neurol. 2022, 13, 897124. [Google Scholar] [CrossRef]
- Hakim, M.S. The Recent Outbreak of Acute and Severe Hepatitis of Unknown Etiology in Children: A Possible Role of Human Adenovirus Infection? J. Med. Virol. 2022, 94, 4065–4068. [Google Scholar] [CrossRef] [PubMed]
- Kozlov, M. Monkeypox Goes Global: Why Scientists Are on Alert. Nature 2022, 606, 15–16. [Google Scholar] [CrossRef]
- Sasaki, T. A Physiolomics Approach to Reveal Systemic Organ Dynamics in a Rodent. Biol. Pharm. Bull. 2019, 42, 1059–1063. [Google Scholar] [CrossRef]
- Rodrigues, E.; Lima, D.; Barbosa, P.; Gonzaga, K.; Guerra, R.O.; Pimentel, M.; Barbosa, H.; Maciel, Á. HRV Monitoring Using Commercial Wearable Devices as a Health Indicator for Older Persons during the Pandemic. Sensors 2022, 22, 2001. [Google Scholar] [CrossRef]
- Hijazi, H.; Abu Talib, M.; Hasasneh, A.; Bou Nassif, A.; Ahmed, N.; Nasir, Q. Wearable Devices, Smartphones, and Interpretable Artificial Intelligence in Combating COVID-19. Sensors 2021, 21, 8424. [Google Scholar] [CrossRef]
- Verma, P.; Pandey, R.K.; Prajapati, P.; Prajapati, V.K. Circulating MicroRNAs: Potential and Emerging Biomarkers for Diagnosis of Human Infectious Diseases. Front. Microbiol. 2016, 7, 1274. [Google Scholar] [CrossRef]
- Frasch, M.G. Heart Rate as a Non-Invasive Biomarker of Inflammation: Implications for Digital Health. Front. Immunol. 2022, 13, 930445. [Google Scholar] [CrossRef]
- Houzet, L.; Yeung, M.L.; de Lame, V.; Desai, D.; Smith, S.M.; Jeang, K.-T. MicroRNA Profile Changes in Human Immunodeficiency Virus Type 1 (HIV-1) Seropositive Individuals. Retrovirology 2008, 5, 118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raihan, M.; Hassan, M.d.M.; Hasan, T.; Bulbul, A.A.-M.; Hasan, M.d.K.; Hossain, M.d.S.; Roy, D.S.; Awal, M.d.A. Development of a Smartphone-Based Expert System for COVID-19 Risk Prediction at Early Stage. Bioengineering 2022, 9, 281. [Google Scholar] [CrossRef] [PubMed]
- Aruleba, R.T.; Adekiya, T.A.; Ayawei, N.; Obaido, G.; Aruleba, K.; Mienye, I.D.; Aruleba, I.; Ogbuokiri, B. COVID-19 Diagnosis: A Review of Rapid Antigen, RT-PCR and Artificial Intelligence Methods. Bioengineering 2022, 9, 153. [Google Scholar] [CrossRef] [PubMed]
- Rodellar, J.; Barrera, K.; Alférez, S.; Boldú, L.; Laguna, J.; Molina, A.; Merino, A. A Deep Learning Approach for the Morphological Recognition of Reactive Lymphocytes in Patients with COVID-19 Infection. Bioengineering 2022, 9, 229. [Google Scholar] [CrossRef]
- Bogunia-Kubik, K.; Wysoczańska, B.; Piątek, D.; Iwaszko, M.; Ciechomska, M.; Świerkot, J. Significance of Polymorphism and Expression of MiR-146a and NFkB1 Genetic Variants in Patients with Rheumatoid Arthritis. Arch. Immunol. Ther. Exp. 2016, 64, 131–136. [Google Scholar] [CrossRef] [Green Version]
- Giuliani, A.; Lattanzi, S.; Ramini, D.; Graciotti, L.; Danni, M.C.; Procopio, A.D.; Silvestrini, M.; Olivieri, F.; Sabbatinelli, J. Potential Prognostic Value of Circulating Inflamma-MiR-146a-5p and MiR-125a-5p in Relapsing-Remitting Multiple Sclerosis. Mult. Scler. Relat. Disord. 2021, 54, 103126. [Google Scholar] [CrossRef]
- Lukiw, W.J. Fission Impossible: Stabilized MiRNA-Based Analogs in Neurodegenerative Disease. Front. Neurosci. 2022, 16, 875957. [Google Scholar] [CrossRef]
- Gidron, Y.; Deschepper, R.; De Couck, M.; Thayer, J.; Velkeniers, B. The Vagus Nerve Can Predict and Possibly Modulate Non-Communicable Chronic Diseases: Introducing a Neuroimmunological Paradigm to Public Health. J. Clin. Med. 2018, 7, 371. [Google Scholar] [CrossRef] [Green Version]
- Shashikant, R.; Chaskar, U.; Phadke, L.; Patil, C. Gaussian Process-Based Kernel as a Diagnostic Model for Prediction of Type 2 Diabetes Mellitus Risk Using Non-Linear Heart Rate Variability Features. Biomed. Eng. Lett. 2021, 11, 273–286. [Google Scholar] [CrossRef]
- Koopman, F.A.; Chavan, S.S.; Miljko, S.; Grazio, S.; Sokolovic, S.; Schuurman, P.R.; Mehta, A.D.; Levine, Y.A.; Faltys, M.; Zitnik, R.; et al. Vagus Nerve Stimulation Inhibits Cytokine Production and Attenuates Disease Severity in Rheumatoid Arthritis. Proc. Natl. Acad. Sci. USA 2016, 113, 8284–8289. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- González, H.F.J.; Yengo-Kahn, A.; Englot, D.J. Vagus Nerve Stimulation for the Treatment of Epilepsy. Neurosurg. Clin. N. Am. 2019, 30, 219–230. [Google Scholar] [CrossRef] [PubMed]
- Drewes, A.; Brock, C.; Rasmussen, S.; Møller, H.; Brock, B.; Deleuran, B.; Farmer, A.; Pfeiffer-Jensen, M. Short-Term Transcutaneous Non-Invasive Vagus Nerve Stimulation May Reduce Disease Activity and pro-Inflammatory Cytokines in Rheumatoid Arthritis: Results of a Pilot Study. Scand. J. Rheumatol. 2021, 50, 20–27. [Google Scholar] [CrossRef] [PubMed]
- Goggins, E.; Mitani, S.; Tanaka, S. Clinical Perspectives on Vagus Nerve Stimulation: Present and Future. Clin. Sci. 2022, 136, 695–709. [Google Scholar] [CrossRef] [PubMed]
- Hao, M.; Liu, X.; Rong, P.; Li, S.; Guo, S.-W. Reduced Vagal Tone in Women with Endometriosis and Auricular Vagus Nerve Stimulation as a Potential Therapeutic Approach. Sci. Rep. 2021, 11, 1345. [Google Scholar] [CrossRef] [PubMed]
- Bendifallah, S.; Suisse, S.; Puchar, A.; Delbos, L.; Poilblanc, M.; Descamps, P.; Golfier, F.; Jornea, L.; Bouteiller, D.; Touboul, C.; et al. Salivary MicroRNA Signature for Diagnosis of Endometriosis. J. Clin. Med. 2022, 11, 612. [Google Scholar] [CrossRef]
- Zhou, T.; Hu, Z.; Yang, S.; Sun, L.; Yu, Z.; Wang, G. Role of Adaptive and Innate Immunity in Type 2 Diabetes Mellitus. J. Diabetes Res. 2018, 2018, 7457269. [Google Scholar] [CrossRef] [PubMed]
- Saariaho, A.-H.; Vuorela, A.; Freitag, T.L.; Pizza, F.; Plazzi, G.; Partinen, M.; Vaarala, O.; Meri, S. Autoantibodies against Ganglioside GM3 Are Associated with Narcolepsy-Cataplexy Developing after Pandemrix Vaccination against 2009 Pandemic H1N1 Type Influenza Virus. J. Autoimmun. 2015, 63, 68–75. [Google Scholar] [CrossRef]
- Jyonouchi, H.; Sun, S.; Le, H. Proinflammatory and Regulatory Cytokine Production Associated with Innate and Adaptive Immune Responses in Children with Autism Spectrum Disorders and Developmental Regression. J. Neuroimmunol. 2001, 120, 170–179. [Google Scholar] [CrossRef]
- Proal, A.D.; VanElzakker, M.B. Long COVID or Post-Acute Sequelae of COVID-19 (PASC): An Overview of Biological Factors That May Contribute to Persistent Symptoms. Front. Microbiol. 2021, 12, 698169. [Google Scholar] [CrossRef]
- VanElzakker, M.B. Chronic Fatigue Syndrome from Vagus Nerve Infection: A Psychoneuroimmunological Hypothesis. Med. Hypotheses 2013, 81, 414–423. [Google Scholar] [CrossRef] [PubMed]
- Sandler, C.X.; Lloyd, A.R. Chronic Fatigue Syndrome: Progress and Possibilities. Med. J. Aust. 2020, 212, 428–433. [Google Scholar] [CrossRef] [PubMed]
- Vreijling, S.R.; Troudart, Y.; Brosschot, J.F. Reduced Heart Rate Variability in Patients With Medically Unexplained Physical Symptoms: A Meta-Analysis of HF-HRV and RMSSD. Psychosom. Med. 2021, 83, 2–15. [Google Scholar] [CrossRef] [PubMed]
- Badran, B.W.; Huffman, S.M.; Dancy, M.; Austelle, C.W.; Bikson, M.; Kautz, S.A.; George, M.S. A Pilot Randomized Controlled Trial of Supervised, at-Home, Self-Administered Transcutaneous Auricular Vagus Nerve Stimulation (TaVNS) to Manage Long COVID Symptoms. Res. Sq. 2022. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rangon, C.-M.; Niezgoda, A. Understanding the Pivotal Role of the Vagus Nerve in Health from Pandemics. Bioengineering 2022, 9, 352. https://doi.org/10.3390/bioengineering9080352
Rangon C-M, Niezgoda A. Understanding the Pivotal Role of the Vagus Nerve in Health from Pandemics. Bioengineering. 2022; 9(8):352. https://doi.org/10.3390/bioengineering9080352
Chicago/Turabian StyleRangon, Claire-Marie, and Adam Niezgoda. 2022. "Understanding the Pivotal Role of the Vagus Nerve in Health from Pandemics" Bioengineering 9, no. 8: 352. https://doi.org/10.3390/bioengineering9080352