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Respiratory viral infections and associated neurological manifestations

  • Shirin Hosseini

    Shirin Hosseini studied biology at the Shahid Beheshti University in Tehran. She obtained her master’s degree in animal physiology at the Ferdowsi University of Mashhad and received her PhD at the Cellular Neurobiology Department of the Technical University of Braunschweig in collaboration with Helmholtz Centre for Infection Research, Braunschweig, Germany. Since 2018, she is working as a postdoctoral researcher at the Cellular Neurobiology Department of Technical University of Braunschweig. Her research focus mainly is on communication between the immune system and the central nervous system. She is interested in the effects of respiratory viral infections on brain function and integrity. In particular, the direct and indirect impact of respiratory viruses on the learning and memory processes and possible therapeutic interventions is her interest.

     ORCID logo     , Kristin Michaelsen-Preusse

    Kristin Michaelsen-Preusse studied biology at the University of Braunschweig. From 2005 to 2009, she was a PhD student at the Institute of Cellular Neuroscience at the Biozentrum in Braunschweig, supervised by Prof. Dr. Martin Korte. In 2009, she moved to Amsterdam where she worked as a postdoctoral fellow at the Netherlands Institute for Neuroscience (NIN) in the group of Dr. Christian Lohmann. In 2011, she returned to Braunschweig where she is working as a senior scientist in the Cellular Neuroscience department headed by Prof. Dr. Martin Korte. Her work is primarily focused on neuronal plasticity where she is interested in synaptic actin dynamics in health and disease (e.g., FXS) as well as the complex interplay between the immune system and the brain.

     ORCID logo     und Martin Korte

    Martin Korte is full professor of Cellular Neurobiology. He studied Biology in Münster, Tübingen and at the NIH, Bethdesda, Maryland, USA. He did his PhD at the MPI for Brain Research in Frankfurt and at the MPI of Psychiatry, Martinsried. He worked afterwards for two years at the Pharmaceutical Company Janssen-Cilag, Neuss. He was then a group leader at the MPI of Neurobiology, Martinsried, and habilitated at the LMU Munich. Since 2004, he is a professor at the TU Braunschweig. He is interested in the cellular processes of learning, memory and forgetting as well as the interaction of the immune system with the nervous system.

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Veröffentlicht/Copyright: 29. März 2021
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Abstract

Respiratory viruses as a major threat to human and animal health today are still a leading cause of worldwide severe pandemics. Although the primary target tissue of these viruses is the lung, they can induce immediate or delayed neuropathological manifestations in humans and animals. Already after the Spanish flu (1918/20) evidence accumulated that neurological diseases can be induced by respiratory viral infections as some patients showed parkinsonism, seizures, or dementia. In the recent outbreak of COVID-19 as well patients suffered from headache, dizziness, nausea, or reduced sense of smell and taste suggesting that SARS-CoV2 may affect the central nervous system (CNS). It was shown that different respiratory viral infections can lead to deleterious complications in the CNS by a direct invasion of the virus into the brain and/or indirect pathways via proinflammatory cytokine expression. Therefore, we will discuss in this review mechanisms how the most prevalent respiratory viruses including influenza and coronaviruses in humans can exert long-lasting detrimental effects on the CNS and possible links to the development of neurodegenerative diseases as an enduring consequence.

Zusammenfassung

Atemwegsviren stellen eine große Bedrohung für die Gesundheit von Mensch und Tier dar und sind eine der Hauptursachen für weltweite schwere Pandemien. Obwohl das primäre Zielgewebe dieser Viren die Lunge ist, können sie bei Mensch und Tier akute oder langfristige neuropathologische Manifestationen auslösen. Bereits nach der Spanischen Grippe (1918/20) gab es zahlreiche Belege dafür, dass neurologische Erkrankungen durch virale Infektionen der Atemwege ausgelöst werden können, da eine Reihe von Patienten Parkinsonismus, epileptische Anfälle oder verschiedene Formen einer Demenz zeigten. Auch beim jüngsten Ausbruch von COVID-19 leiden die Patienten unter Kopfschmerzen, Schwindel, Übelkeit oder vermindertem Geruchs- und Geschmackssinn, was darauf hindeutet, dass SARS-CoV2 das Zentralnervensystem (CNS) beeinträchtigen könnte. Es konnte gezeigt werden, dass verschiedene respiratorische Virusinfektionen zu schädlichen Komplikationen im CNS führen, und zwar durch eine direkte Invasion des Virus in das Gehirn und/oder indirekte Wege über eine proinflammatorische Zytokinexpression. Daher werden wir in dieser Übersicht Mechanismen diskutieren, wie die beim Menschen am weitesten verbreiteten respiratorischen Viren, darunter Influenza- und Coronaviren, negative Auswirkungen auf das CNS haben können und so eine mögliche Verbindung zur Entwicklung neurodegenerativer Erkrankungen als Langzeitfolge haben.

Keywords: central nervous system; coronavirus; influenza virus; neurodegeneration; respiratory viral infections
Schlüsselwörter: Zentralnervensystem; Coronavirus; Influenzavirus; Neurodegeneration; Respiratorische Virusinfektionen
Corresponding author: Martin Korte, Department of Cellular Neurobiology, Zoological Institute, TU Braunschweig, Spielmannstraße 7, 38106Braunschweig, Germany; and Helmholtz Centre for Infection Research, Neuroinflammation and Neurodegeneration Group, Braunschweig, Germany, E-mail:

About the authors

Shirin Hosseini

Shirin Hosseini studied biology at the Shahid Beheshti University in Tehran. She obtained her master’s degree in animal physiology at the Ferdowsi University of Mashhad and received her PhD at the Cellular Neurobiology Department of the Technical University of Braunschweig in collaboration with Helmholtz Centre for Infection Research, Braunschweig, Germany. Since 2018, she is working as a postdoctoral researcher at the Cellular Neurobiology Department of Technical University of Braunschweig. Her research focus mainly is on communication between the immune system and the central nervous system. She is interested in the effects of respiratory viral infections on brain function and integrity. In particular, the direct and indirect impact of respiratory viruses on the learning and memory processes and possible therapeutic interventions is her interest.

Kristin Michaelsen-Preusse

Kristin Michaelsen-Preusse studied biology at the University of Braunschweig. From 2005 to 2009, she was a PhD student at the Institute of Cellular Neuroscience at the Biozentrum in Braunschweig, supervised by Prof. Dr. Martin Korte. In 2009, she moved to Amsterdam where she worked as a postdoctoral fellow at the Netherlands Institute for Neuroscience (NIN) in the group of Dr. Christian Lohmann. In 2011, she returned to Braunschweig where she is working as a senior scientist in the Cellular Neuroscience department headed by Prof. Dr. Martin Korte. Her work is primarily focused on neuronal plasticity where she is interested in synaptic actin dynamics in health and disease (e.g., FXS) as well as the complex interplay between the immune system and the brain.

Martin Korte

Martin Korte is full professor of Cellular Neurobiology. He studied Biology in Münster, Tübingen and at the NIH, Bethdesda, Maryland, USA. He did his PhD at the MPI for Brain Research in Frankfurt and at the MPI of Psychiatry, Martinsried. He worked afterwards for two years at the Pharmaceutical Company Janssen-Cilag, Neuss. He was then a group leader at the MPI of Neurobiology, Martinsried, and habilitated at the LMU Munich. Since 2004, he is a professor at the TU Braunschweig. He is interested in the cellular processes of learning, memory and forgetting as well as the interaction of the immune system with the nervous system.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: None declared.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Algahtani, H., Subahi, A., and Shirah, B. (2016). Neurological complications of Middle East respiratory syndrome coronavirus: a report of two cases and review of the literature. Case Rep. Neurol. Med.2016, 3502683.10.1155/2016/3502683Suche in Google Scholar PubMed PubMed Central

Alshebri, M.S., Alshouimi, R.A., Alhumidi, H.A., and Alshaya, A.I. (2020). Neurological complications of SARS-CoV, MERS-CoV, and COVID-19. SN Compr. Clin. Medi., 1–11, https://doi.org/10.1007/s42399-020-00589-2.Suche in Google Scholar PubMed PubMed Central

Arbour, N., Day, R., Newcombe, J., and Talbot, P.J. (2000). Neuroinvasion by human respiratory coronaviruses. J. Virol.74, 8913.10.1128/JVI.74.19.8913-8921.2000Suche in Google Scholar PubMed PubMed Central

Atluri, V.S., Hidalgo, M., Samikkannu, T., Kurapati, K.R., and Nair, M. (2015). Synaptic plasticity and neurological disorders in neurotropic viral infections. Neural Plast.2015, 138979.10.1155/2015/138979Suche in Google Scholar PubMed PubMed Central

Baig, A.M., Khaleeq, A., Ali, U., and Syeda, H. (2020). Evidence of the COVID-19 virus targeting the CNS: tissue distribution, host–virus interaction, and proposed neurotropic mechanisms. ACS Chem. Neurosci.11, 995–998, https://doi.org/10.1021/acschemneuro.0c00122.Suche in Google Scholar PubMed PubMed Central

Barbosa-Silva, M.C., Santos, L.E., and Rangel, B. (2018). The impact of non-neurotropic influenza strains on the brain: a role for microglial priming? J. Neurosci.: Off. J. Soc. Neurosci.38, 7758–7760.10.1523/JNEUROSCI.1368-18.2018Suche in Google Scholar PubMed PubMed Central

Berry, M., Gamieldien, J., and Fielding, B.C. (2015). Identification of new respiratory viruses in the new millennium. Viruses7, 996–1019.10.3390/v7030996Suche in Google Scholar PubMed PubMed Central

Bohmwald, K., Galvez, N., Ríos, M., and Kalergis, A.M. (2018). Neurologic alterations due to respiratory virus infections. Front. Cell. Neurosci.12, 386.10.3389/fncel.2018.00386Suche in Google Scholar PubMed PubMed Central

Castelli, V., Cimini, A., and Ferri, C. (2020). Cytokine storm in COVID-19: “when you come out of the storm, you won’t be the same person who walked in”. Front. Immunol.11, 2132, https://doi.org/10.3389/fimmu.2020.02132.Suche in Google Scholar PubMed PubMed Central

Cornelius, A.D.A., Hosseini, S., Schreier, S., Fritzsch, D., Weichert, L., Michaelsen-Preusse, K., Fendt, M., and Kröger, A. (2020). Langat virus infection affects hippocampal neuron morphology and function in mice without disease signs. J. Neuroinflammation17, 278.10.1186/s12974-020-01951-wSuche in Google Scholar PubMed PubMed Central

Desforges, M., Le Coupanec, A., Dubeau, P., Bourgouin, A., Lajoie, L., Dubé, M., and Talbot, P.J. (2020). Human coronaviruses and other respiratory viruses: underestimated opportunistic pathogens of the central nervous system? Viruses12, 14.10.3390/v12010014Suche in Google Scholar PubMed PubMed Central

Ekstrand, J.J. (2012). Neurologic complications of influenza. Semin. Pediatr. Neurol.19, 96–100.10.1016/j.spen.2012.02.004Suche in Google Scholar PubMed

Engelhardt, B. and Sorokin, L. (2009). The blood-brain and the blood-cerebrospinal fluid barriers: function and dysfunction. Semin. Immunopathol.31, 497–511.10.1007/s00281-009-0177-0Suche in Google Scholar PubMed

Gamboa, E.T., Wolf, A., Yahr, M.D., Harter, D.H., Duffy, P.E., Barden, H., and Hsu, K.C. (1974). Influenza virus antigen in postencephalitic parkinsonism brain: detection by immunofluorescence. Arch. Neurol.31, 228–232.10.1001/archneur.1974.00490400042003Suche in Google Scholar PubMed

Groves, H.T., Higham, S.L., Moffatt, M.F., Cox, M.J., and Tregoning, J.S. (2020). Respiratory viral infection alters the gut microbiota by inducing inappetence. mBio.11, e03236-19, https://doi.org/10.1128/mBio.03236-19.Suche in Google Scholar PubMed PubMed Central

Henry, J., Smeyne, R.J., Jang, H., Miller, B., and Okun, M.S. (2010). Parkinsonism and neurological manifestations of influenza throughout the 20th and 21st centuries. Park. Relat. Disord.16, 566–571.10.1016/j.parkreldis.2010.06.012Suche in Google Scholar PubMed PubMed Central

Hosseini, S., Michaelsen-Preusse, K., Grigoryan, G., Chhatbar, C., Kalinke, U., and Korte, M. (2020). Type I interferon receptor signaling in astrocytes regulates hippocampal synaptic plasticity and cognitive function of the healthy CNS. Cell Rep.31, 107666.10.1016/j.celrep.2020.107666Suche in Google Scholar PubMed

Hosseini, S., Wilk, E., Michaelsen-Preusse, K., Gerhauser, I., Baumgärtner, W., Geffers, R., Schughart, K., and Korte, M. (2018). Long-term neuroinflammation induced by influenza A virus infection and the impact on hippocampal neuron morphology and function. J. Neurosci.: Off. J. Soc. Neurosci.38, 3060.10.1523/JNEUROSCI.1740-17.2018Suche in Google Scholar PubMed PubMed Central

Jang, H., Boltz, D., McClaren, J., Pani, A.K., Smeyne, M., Korff, A., Webster, R., and Smeyne, R.J. (2012). Inflammatory effects of highly pathogenic H5N1 influenza virus infection in the CNS of mice. J. Neurosci.: Off. J. Soc. Neurosci.32, 1545–1559.10.1523/JNEUROSCI.5123-11.2012Suche in Google Scholar PubMed PubMed Central

Jang, H., Boltz, D., Sturm-Ramirez, K., Shepherd, K.R., Jiao, Y., Webster, R., and Smeyne, R.J. (2009). Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc. Natl. Acad. Sci. Unit. States Am.106, 14063–14068.10.1073/pnas.0900096106Suche in Google Scholar PubMed PubMed Central

Jurgens, H.A., Amancherla, K., and Johnson, R.W. (2012). Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J. Neurosci. : Off. J. Soc. Neurosci.32, 3958–3968.10.1523/JNEUROSCI.6389-11.2012Suche in Google Scholar PubMed PubMed Central

Kaplan, L., Chow, B.W., and Gu, C. (2020). Neuronal regulation of the blood-brain barrier and neurovascular coupling. Nat. Rev. Neurosci.21, 416–432.10.1038/s41583-020-0322-2Suche in Google Scholar PubMed PubMed Central

Khandaker, G., Zurynski, Y., Buttery, J., Marshall, H., Richmond, P.C., Dale, R.C., Royle, J., Gold, M., Snelling, T., Whitehead, B., et al.. (2012). Neurologic complications of influenza A(H1N1)pdm09: surveillance in 6 pediatric hospitals. Neurology79, 1474–1481.10.1212/WNL.0b013e31826d5ea7Suche in Google Scholar PubMed PubMed Central

Kim, Y.K. and Shin, C. (2018). The microbiota-gut-brain Axis in neuropsychiatric disorders: pathophysiological mechanisms and novel treatments. Curr. Neuropharmacol.16, 559–573.10.2174/1570159X15666170915141036Suche in Google Scholar PubMed PubMed Central

Korte, M. and Schmitz, D. (2016). Cellular and system biology of memory: timing, molecules, and beyond. Physiol. Rev.96, 647–693.10.1152/physrev.00010.2015Suche in Google Scholar PubMed

Koyuncu, O.O., Hogue, I.B., and Enquist, L.W. (2013). Virus infections in the nervous system. Cell Host Microbe13, 379–393.10.1016/j.chom.2013.03.010Suche in Google Scholar PubMed PubMed Central

Krauthausen, M., Kummer, M.P., Zimmermann, J., Reyes-Irisarri, E., Terwel, D., Bulic, B., Heneka, M.T., and Müller, M. (2015). CXCR3 promotes plaque formation and behavioral deficits in an Alzheimer’s disease model. J. Clin. Invest.125, 365–378.10.1172/JCI66771Suche in Google Scholar PubMed PubMed Central

Li, Y.C., Bai, W.Z., and Hashikawa, T. (2020). The neuroinvasive potential of SARS‐CoV2 may be at least partially responsible for the respiratory failure of COVID‐19 patients. J. Med. Virol.92, 552–555, https://doi.org/10.1002/jmv.25728.Suche in Google Scholar PubMed PubMed Central

Li, Y., Fu, L., Gonzales, D.M., and Lavi, E. (2004). Coronavirus neurovirulence correlates with the ability of the virus to induce proinflammatory cytokine signals from astrocytes and microglia. J. Virol.78, 3398–3406.10.1128/JVI.78.7.3398-3406.2004Suche in Google Scholar PubMed PubMed Central

Li, Y., Li, H., Fan, R., Wen, B., Zhang, J., Cao, X., Wang, C., Song, Z., Li, S., and Li, X. (2016). Coronavirus infections in the central nervous system and respiratory tract show distinct features in hospitalized children. Intervirology59, 163–169.10.1159/000453066Suche in Google Scholar PubMed PubMed Central

Louveau, A., Harris, T.H., and Kipnis, J. (2015). Revisiting the mechanisms of CNS immune privilege. Trends Immunol.36, 569–577.10.1016/j.it.2015.08.006Suche in Google Scholar PubMed PubMed Central

Ludlow, M., Kortekaas, J., Herden, C., Hoffmann, B., Tappe, D., Trebst, C., Griffin, D.E., Brindle, H.E., Solomon, T., Brown, A.S., et al.. (2016). Neurotropic virus infections as the cause of immediate and delayed neuropathology. Acta Neuropathol.131, 159–184.10.1007/s00401-015-1511-3Suche in Google Scholar PubMed PubMed Central

Lynch, M.A. (2002). Interleukin-1β exerts a myriad of effects in the brain and in particular in the hippocampus: analysis of some of these actions. Vitam. Horm.64, 185–219.10.1016/S0083-6729(02)64006-3Suche in Google Scholar

Madden, K. (2003). West Nile virus infection and its neurological manifestations. Clin. Med. Res.1, 145–150.10.3121/cmr.1.2.145Suche in Google Scholar PubMed PubMed Central

Marreiros, R., Müller-Schiffmann, A., Trossbach, S.V., Prikulis, I., Hänsch, S., Weidtkamp-Peters, S., Moreira, A.R., Sahu, S., Soloviev, I., Selvarajah, S., et al.. (2020). Disruption of cellular proteostasis by H1N1 influenza A virus causes α-synuclein aggregation. Proc. Natl. Acad. Sci. Unit. States Am.117, 6741–6751.10.1073/pnas.1906466117Suche in Google Scholar PubMed PubMed Central

McGavern, D.B. and Kang, S.S. (2011). Illuminating viral infections in the nervous system. Nat. Rev. Immunol.11, 318–329.10.1038/nri2971Suche in Google Scholar PubMed PubMed Central

Meinhardt, J., Radke, J., Dittmayer, C., Franz, J., Thomas, C., Mothes, R., Laue, M., Schneider, J., Brünink, S., and Greuel, S., et al.. (2021). Olfactory transmucosal SARS-CoV-2 invasion as a port of central nervous system entry in individuals with COVID-19. Nat. Neurosci.24, 168–175, https://doi.org/10.1038/s41593-020-00758-5.Suche in Google Scholar PubMed

Moro, E., Priori, A., Beghi, E., Helbok, R., Campiglio, L., Bassetti, C.L., Bianchi, E., Maia, L.F., Ozturk, S., Cavallieri, F., et al.. (2020). The international European Academy of Neurology survey on neurological symptoms in patients with COVID-19 infection. Eur. J. Neurol.27, 1727–1737.10.1111/ene.14407Suche in Google Scholar PubMed PubMed Central

Mylonaki, E., Harrer, A., Pilz, G., Stalzer, P., Otto, F., Trinka, E., and Wipfler, P. (2020). Neurological complications associated with influenza in season 2017/18 in Austria- a retrospective single center study. J. Clin. Virol.: Off. Publ. Pan Am. Soc. Clin. Virol.127, 104340.10.1016/j.jcv.2020.104340Suche in Google Scholar PubMed

Netland, J., Meyerholz, D.K., Moore, S., Cassell, M., and Perlman, S. (2008). Severe acute respiratory syndrome coronavirus infection causes neuronal death in the absence of encephalitis in mice transgenic for human ACE2. J. Virol.82, 7264–7275.10.1128/JVI.00737-08Suche in Google Scholar PubMed PubMed Central

Ng Kee Kwong, K.C., Mehta, P.R., Shukla, G., and Mehta, A.R. (2020). COVID-19, SARS and MERS: a neurological perspective. J. Clin. Neurosci.: Off. J. Neurosurg. Soc. Australas.77, 13–16.10.1016/j.jocn.2020.04.124Suche in Google Scholar PubMed PubMed Central

Ng, Y.P., Yip, T.F., Peiris, J.S.M., Ip, N.Y., and Lee, S.M.Y. (2018). Avian influenza A H7N9 virus infects human astrocytes and neuronal cells and induces inflammatory immune responses. J. Neurovirol.24, 752–760.10.1007/s13365-018-0659-8Suche in Google Scholar PubMed PubMed Central

Nichols, W.G., Campbell, A.J.P., and Boeckh, M. (2008). Respiratory viruses other than influenza virus: impact and therapeutic advances. Clin. Microbiol. Rev.21, 274–290.10.1128/CMR.00045-07Suche in Google Scholar PubMed PubMed Central

Park, C., Ishinaka, M., Takada, A., Kida, H., Kimura, T., Ochiai, K., and Umemura, T. (2002). The invasion routes of neurovirulent A/Hong Kong/483/97 (H5N1) influenza virus into the central nervous system after respiratory infection in mice. Arch. Virol.147, 1425–1436.10.1007/s00705-001-0750-xSuche in Google Scholar PubMed

Paterson, R.W., Brown, R.L., Benjamin, L., Nortley, R., Wiethoff, S., Bharucha, T., Jayaseelan, D.L., Kumar, G., Raftopoulos, R.E., and Zambreanu, L., et al.. (2020). The emerging spectrum of COVID-19 neurology: clinical, radiological and laboratory findings. Brain: J. Neurol.143, 3104–3120, https://doi.org/10.1093/brain/awaa240.Suche in Google Scholar PubMed PubMed Central

Perlman, S. and Wheeler, D.L. (2016). Neurotropic coronavirus infections. Neurotropic viral infections: volume 1: neurotropic RNA viruses. Reiss, C.S., ed. (Cham: Springer International Publishing), pp. 115–148.10.1007/978-3-319-33133-1_5Suche in Google Scholar

Pezzini, A. and Padovani, A. (2020). Lifting the mask on neurological manifestations of COVID-19. Nat. Rev. Neurol.16, 636–644.10.1038/s41582-020-0398-3Suche in Google Scholar PubMed PubMed Central

Prieto, G.A. and Cotman, C.W. (2017). Cytokines and cytokine networks target neurons to modulate long-term potentiation. Cytokine Growth Factor Rev.34, 27–33.10.1016/j.cytogfr.2017.03.005Suche in Google Scholar PubMed PubMed Central

Riazi, K., Galic, M.A., Kentner, A.C., Reid, A.Y., Sharkey, K.A., and Pittman, Q.J. (2015). Microglia-dependent alteration of glutamatergic synaptic transmission and plasticity in the hippocampus during peripheral inflammation. Clin. Infect. Dis.: An Off. Publ. Infect. Dis. Soc. Am.35, 4942–4952.10.1523/JNEUROSCI.4485-14.2015Suche in Google Scholar PubMed PubMed Central

Robinson, C.P. and Busl, K.M. (2020). Neurologic manifestations of severe respiratory viral contagions. Crit. Care Explor.2, e0107.10.1097/CCE.0000000000000107Suche in Google Scholar PubMed PubMed Central

Sadasivan, S., Zanin, M., O’Brien, K., Schultz-Cherry, S., and Smeyne, R.J. (2015). Induction of microglia activation after infection with the non-neurotropic A/CA/04/2009 H1N1 influenza virus. PloS One10, e0124047.10.1371/journal.pone.0124047Suche in Google Scholar PubMed PubMed Central

Santos, L.E., Beckman, D., and Ferreira, S.T. (2016). Microglial dysfunction connects depression and Alzheimer’s disease. Brain Behav. Immun.55, 151–165.10.1016/j.bbi.2015.11.011Suche in Google Scholar PubMed

Sips, G.J., Wilschut, J., and Smit, J.M. (2012). Neuroinvasive flavivirus infections. Rev. Med. Virol.22, 69–87.10.1002/rmv.712Suche in Google Scholar PubMed

Sulzer, D., Antonini, A., Leta, V., Nordvig, A., Smeyne, R.J., Goldman, J.E., Al-Dalahmah, O., Zecca, L., Sette, A., Bubacco, L., et al.. (2020). COVID-19 and possible links with Parkinson’s disease and parkinsonism: from bench to bedside. NPJ Parkinson’s Dis.6, 18.10.1038/s41531-020-00123-0Suche in Google Scholar PubMed PubMed Central

Swanson, P.A. and McGavern, D.B. (2015). Viral diseases of the central nervous system. Curr. Opin. Virol.11, 44–54.10.1016/j.coviro.2014.12.009Suche in Google Scholar PubMed PubMed Central

Teijaro, J.R., Walsh, K.B., Cahalan, S., Fremgen, D.M., Roberts, E., Scott, F., Martinborough, E., Peach, R., Oldstone, M.B., and Rosen, H. (2011). Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell146, 980–991.10.1016/j.cell.2011.08.015Suche in Google Scholar PubMed PubMed Central

Tisoncik, J.R., Korth, M.J., Simmons, C.P., Farrar, J., Martin, T.R., and Katze, M.G. (2012). Into the eye of the cytokine storm. Microbiol. Mol. Biol. Rev. : MMBR76, 16–32.10.1128/MMBR.05015-11Suche in Google Scholar PubMed PubMed Central

Toovey, S., Jick, S.S., and Meier, C.R. (2011). Parkinson’s disease or Parkinson symptoms following seasonal influenza. Influenza Other Respir. Viruses5, 328–333.10.1111/j.1750-2659.2011.00232.xSuche in Google Scholar PubMed PubMed Central

Troy, N.M. and Bosco, A. (2016). Respiratory viral infections and host responses; insights from genomics. Respir. Res.17, 156.10.1186/s12931-016-0474-9Suche in Google Scholar PubMed PubMed Central

Vasek, M.J., Garber, C., Dorsey, D., Durrant, D.M., Bollman, B., Soung, A., Yu, J., Perez-Torres, C., Frouin, A., and Wilton, D.K. (2016). A complement–microglial axis drives synapse loss during virus-induced memory impairment. Nature534, 538–543.10.1038/nature18283Suche in Google Scholar PubMed PubMed Central

Verstrepen, K., Baisier, L., and De Cauwer, H. (2020). Neurological manifestations of COVID-19, SARS and MERS. Acta Neurol. Belg.120, 1051–1060.10.1007/s13760-020-01412-4Suche in Google Scholar PubMed PubMed Central

Vezzani, A., Fujinami, R.S., White, H.S., Preux, P.M., Blümcke, I., Sander, J.W., and Löscher, W. (2016). Infections, inflammation and epilepsy. Acta Neuropathol.131, 211–234.10.1007/s00401-015-1481-5Suche in Google Scholar PubMed PubMed Central

Vitkovic, L., Konsman, J.P., Bockaert, J., Dantzer, R., Homburger, V., and Jacque, C. (2000). Cytokine signals propagate through the brain. Mol. Psychiatr.5, 604–615.10.1038/sj.mp.4000813Suche in Google Scholar PubMed

Xia, H. and Lazartigues, E. (2008). Angiotensin‐converting enzyme 2 in the brain: properties and future directions. J. Neurochem.107, 1482–1494.10.1111/j.1471-4159.2008.05723.xSuche in Google Scholar PubMed PubMed Central

Xu, J., Zhong, S., Liu, J., Li, L., Li, Y., Wu, X., Li, Z., Deng, P., Zhang, J., Zhong, N., et al.. (2005). Detection of severe acute respiratory syndrome coronavirus in the brain: potential role of the chemokine mig in pathogenesis. Clin. Infect. Dis.: An Off. Publ. Infect. Dis. Soc. Am.41, 1089–1096.10.1086/444461Suche in Google Scholar PubMed PubMed Central

Yu, M., Zhang, K., Qi, W., Huang, Z., Ye, J., Ma, Y., Liao, M., and Ning, Z. (2014). Expression pattern of NLRP3 and its related cytokines in the lung and brain of avian influenza virus H9N2 infected BALB/c mice. Virol. J.11, 229.10.1186/s12985-014-0229-5Suche in Google Scholar PubMed PubMed Central

Published Online: 2021-03-29
Published in Print: 2021-05-26

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Artikel in diesem Heft

  1. Frontmatter
  2. Editorial
  3. Editorial der neuen NWG-Präsidenten zum Amtsantritt
  4. Review articles
  5. Respiratory viral infections and associated neurological manifestations
  6. Nanoscale imaging of the functional anatomy of the brain
  7. Mental health and biological evolution: implications for psychiatry and psychosomatic medicine
  8. Neurons interact with the microbiome: an evolutionary-informed perspective
  9. Presentation of scientific institutions
  10. Innovative retinal interfaces for optimized artificial vision – a new DFG funded Research Training Group
  11. ALBA Network – towards diversity and equity in brain sciences
  12. Obituary
  13. Nachruf Dr. Jan Kunze (1968–2021)
  14. Nachrichten aus der Gesellschaft
  15. Who is who im Vorstand der Neurowissenschaftlichen Gesellschaft – die neuen Vorstandsmitglieder stellen sich vor
https://doi.org/10.1515/nf-2020-0035
Schlagwörter für diesen Artikel
central nervous system; coronavirus; influenza virus; neurodegeneration; respiratory viral infections

Artikel in diesem Heft

  1. Frontmatter
  2. Editorial
  3. Editorial der neuen NWG-Präsidenten zum Amtsantritt
  4. Review articles
  5. Respiratory viral infections and associated neurological manifestations
  6. Nanoscale imaging of the functional anatomy of the brain
  7. Mental health and biological evolution: implications for psychiatry and psychosomatic medicine
  8. Neurons interact with the microbiome: an evolutionary-informed perspective
  9. Presentation of scientific institutions
  10. Innovative retinal interfaces for optimized artificial vision – a new DFG funded Research Training Group
  11. ALBA Network – towards diversity and equity in brain sciences
  12. Obituary
  13. Nachruf Dr. Jan Kunze (1968–2021)
  14. Nachrichten aus der Gesellschaft
  15. Who is who im Vorstand der Neurowissenschaftlichen Gesellschaft – die neuen Vorstandsmitglieder stellen sich vor
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Heruntergeladen am 7.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/nf-2020-0035/html
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