Long-Term Neuroinflammation Induced by Influenza A Virus Infection and the Impact on Hippocampal Neuron Morphology and Function
Open accessAbstract
Acute influenza infection has been reported to be associated with neurological symptoms. However, the long-term consequences of an infection with neurotropic and non-neurotropic influenza A virus (IAV) variants for the CNS remain elusive. We can show that spine loss in the hippocampus after infection with neurotropic H7N7 (rSC35M) and non-neurotropic H3N2 (maHK68) in female C57BL/6 mice persists well beyond the acute phase of the disease. Although spine number was significantly reduced at 30 d postinfection (dpi) with H7N7 or H3N2, full recovery could only be observed much later at 120 dpi. Infection with H1N1 virus, which was shown previously to affect spine number and hippocampus-dependent learning acutely, had no significant long-term effects. Spine loss was associated with an increase in the number of activated microglia, reduced long-term potentiation in the hippocampus, and impairment in spatial memory formation, indicating that IAV-associated inflammation induced functional and structural alterations in hippocampal networks. Transcriptome analyses revealed regulation of many inflammatory and neuron- and glia-specific genes in H3N2- and H7N7-infected mice at day 18 and in H7N7-infected mice at day 30 pi that related to the structural and functional alterations. Our data provide evidence that neuroinflammation induced by neurotropic H7N7 and infection of the lung with a non-neurotropic H3N2 IAV result in long-term impairments in the CNS. IAV infection in humans may therefore not only lead to short-term responses in infected organs, but may also trigger neuroinflammation and associated chronic alterations in the CNS. SIGNIFICANCE STATEMENT In the acute phase of influenza infection, neuroinflammation can lead to alterations in hippocampal neuronal morphology and cognitive deficits. The results of this study now also provide evidence that neuroinflammation induced by influenza A virus (IAV) infection can induce longer-lasting, virus-specific alterations in neuronal connectivity that are still detectable 1 month after infection and are associated with impairments in spatial memory formation. IAV infection in humans may therefore not only lead to short-term responses in infected organs, but may also trigger neuroinflammation and associated chronic alterations in the CNS.
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Influenza infection may enter the brain through several routes or send deleterious signals to the brain via sensory neurons and trigger neuroinflammation or associated chronic alterations in the CNS.
“Influenza infection may enter the brain through several routes [122,123] or send deleterious signals to the brain via sensory neurons [124] and trigger neuroinflammation or associated chronic alterations in the CNS [125].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [125]
There is a precedent for acute viral infections causing long-term inflammation and dysfunction that predisposes individuals to neurodegenerative disease.
“There is a precedent for acute viral infections causing long-term inflammation and dysfunction that predisposes individuals to neurodegenerative disease44,45”
From Dysregulation of brain and choroid plexus cell types in severe COVID-19 (2021) · cites this paper as [44]
Cognitive impairment may be caused by viral infections associated with direct invasion of the central nervous system, or as an indirect effect of systemic infections not typically causing CNS infection.
“Cognitive impairment may be caused by viral infections associated with direct invasion of the central nervous system [11, 24], or as an indirect effect of systemic infections not typically causing CNS infection (e.g. cytokine storm, neuro-inflammation, hypercoagulability) [11, 24].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [11]
Mechanisms underlying viral pathogenesis in these conditions may include a direct viral effect or indirect mechanisms, such as inflammation, epigenetic changes, and hypercoagulable changes, that may impact brain structure and function in healthy or cognitively impaired individuals.
“Mechanisms underlying viral pathogenesis in these conditions may include a direct viral effect or indirect mechanisms, such as inflammation, epigenetic changes, and hypercoagulable changes, that may impact on brain structure and function in healthy or in cognitively impaired individuals [6, 11–15].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [11]
The H1N1 strain of influenza causes acute elevation in CNS cytokines, hippocampal microglial reactivity, and impaired performance in cognitive behavioral tests.
“The H1N1 strain of influenza, which is not neuroinvasive in mouse models, causes acute elevation in CNS cytokines, hippocampal microglial reactivity, and impaired performance in cognitive behavioral tests (Hosseini et al., 2018; Jurgens et al., 2012).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Hosseini et al., 2018
Other viral syndromes such as influenza can cause microglial reactivity, elevated CNS cytokine levels, and impair cognitive function, even in the absence of neuroinvasion.
“Other viral syndromes such as influenza can cause microglial reactivity, elevated CNS cytokine levels, and impair cognitive function, even in the absence of neuroinvasion (Hosseini et al., 2018; Jurgens et al., 2012).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Hosseini et al., 2018
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Hristovska, I., & Pascual, O. (2016) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00073 · Cited by 92 · cited 1× · see citing works
“Therefore, long-term microglial activation might interfere with these processes (Nimmerjahn et al., 2005; Yirmiya and Goshen, 2011; Hristovska and Pascual, 2015).”
BackgroundCamara, M. L., Corrigan, F., Jaehne, E. J., Jawahar, M. C., Anscomb, H., & Baune, B. T. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.199 · Cited by 91 · see citing works
Richwine, A. F., Parkin, A. O., Buchanan, J. B., Chen, J., Markham, J. A., Juraska, J. M., & Johnson, R. W. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.08.003 · Cited by 87 · cited 18× · see citing works
“Indeed, it is now well established that a peripheral immune stimulation can affect the intact CNS (Richwine et al., 2008) via the activation of microglia during a secondary, mirror inflammatory response in the brain (Riazi et al., 2015).”
BackgroundInfluentialLovell, M. A. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-0992 · Cited by 87 · see citing works
Rubin, S. A., Sylves, P., Vogel, M. W., Pletnikov, M., Moran, T. H., Schwartz, G. J., & Carbone, K. M. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00133-6 · Cited by 83 · cited 1× · see citing works
“It was indeed shown previously that the progressive nature of neurotropic virus-induced damage in the dentate gyrus (DG), such as during Borna virus infection, is associated with impaired performance in the Morris water maze (Rubin et al., 1999).”
BackgroundRBFOX3/NeuN is Required for Hippocampal Circuit Balance and Function
Wang, H., Hsieh, P.-F., Huang, D.-F., Chin, P.-S., Chou, C., Tung, C.-C., Chen, S.-Y., Lee, L., Gau, S. S., & Huang, H. (2015) · Scientific Reports · doi:10.1038/srep17383 · Cited by 78 · cited 1× · see citing works
“In addition, Rbfox3 knock-out mice show deficits in synaptic transmission and plasticity in the DG (Wang et al., 2015).”
BackgroundLin, Y.-S., Wang, H., Huang, D.-F., Hsieh, P.-F., Lin, M.-Y., Chou, C., Wu, I.-J., Huang, G., Gau, S. S., & Huang, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164164 · Cited by 75 · cited 1× · see citing works
“Dysfunction of these genes has been identified in several neurodevelopmental and neuropsychiatric disorders such as autism, schizophrenia, and cognitive impairments (Demyanenko et al., 2014; Lee et al., 2016; Lin et al., 2016).”
BackgroundNuttall, J. R., & Oteiza, P. I. (2013) · Genes & Nutrition · doi:10.1007/s12263-013-0379-x · Cited by 74 · see citing works
Lynch, M. A. (2002) · Vitamins and hormones · doi:10.1016/s0083-6729(02)64006-3 · Cited by 71 · see citing works
Inflammatory monocytes damage the hippocampus during acute picornavirus infection of the brain
Howe, C. L., LaFrance-Corey, R. G., Sundsbak, R. S., & LaFrance, S. J. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-50 · Cited by 62 · cited 1× · see citing works
“, IL-1 , IL-6, TNF- , and IFN- ) can be observed across multiple brain regions, including the hippocampus (Howe et al., 2012; Elmore et al., 2014; Heneka et al., 2014; Klein et al., 2017).”
BackgroundMajde, J. A., Bohnet, S. G., Ellis, G., Churchill, L., Leyva-Grado, V. H., Wu, M., Szentirmai, É., Rehman, A., & Krueger, J. M. (2007) · Journal of NeuroVirology · doi:10.1080/13550280701427069 · Cited by 62 · cited 2× · see citing works
“First, we used the well characterized PR8 (A/PuertoRico/8/34) nonneurotropic virus (Majde et al., 2007; Hodgson et al., 2012).”
BackgroundMethodCooper, D. S., Saxena, N., Yang, H. S., Lee, H., Moring, A. G., Lee, A., & Choi, I. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m408646200 · Cited by 61 · see citing works
Cell Adhesion Molecules: An Overview
Joseph‐Silverstein, J., & Silverstein, R. L. (1998) · Cancer Investigation · doi:10.3109/07357909809050034 · Cited by 57 · see citing works
Virus-induced neurobehavioral disorders: mechanisms and implications
Tomonaga, K. (2004) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2003.12.001 · Cited by 56 · cited 1× · see citing works
“Neurotropic IAV strains are indeed able to enter the CNS through the blood– brain barrier (BBB) or microvascular endothelial cells (Tomonaga, 2004).”
BackgroundThe Neuropsychiatric Disease-Associated Genecacna1cMediates Survival of Young Hippocampal Neurons
Lee, A. S., Jesús‐Cortés, H. D., Kabir, Z. D., Knobbe, W., Orr, M., Burgdorf, C. E., Huntington, P. J., McDaniel, L., Britt, J. K., Hoffmann, F., et al. (2016) · eNeuro · doi:10.1523/eneuro.0006-16.2016 · Cited by 56 · see citing works
Leist, S. R., Pilzner, C., van den Brand, J. M. A., Dengler, L., Geffers, R., Kuiken, T., Balling, R., Kollmus, H., & Schughart, K. (2016) · BMC Genomics · doi:10.1186/s12864-016-2483-y · Cited by 53 · cited 1× · see citing works
“, 1979) in our studies, for which we established a well characterized mouse model (Leist et al., 2016).”
BackgroundSelf-citationSex differences in murine susceptibility to systemic viral infections
Geurs, T. L., Hill, E. B., Lippold, D., & French, A. R. (2011) · Journal of Autoimmunity · doi:10.1016/j.jaut.2011.12.003 · Cited by 50 · cited 1× · see citing works
“Earlier studies demonstrated that female mice are more susceptible and produce more neutralizing antibodies and higher levels of chemokines and cytokines than males during infection with influenza viruses (Geurs et al., 2012), so only female mice were used in this study.”
MethodPolicing the Police: Astrocytes Modulate Microglial Activation
Shih, A. Y., Fernandes, H., Choi, F. Y., Kozoriz, M. G., Liu, Y.-R., Li, P., Cowan, C., & Klegeris, A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0936-06.2006 · Cited by 49 · see citing works
Majumdar, D., & Bevensee, M. O. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.09.037 · Cited by 49 · see citing works
Haller, O., Arnheiter, H., & Lindenmann, J.-M. (1979) · The Journal of Experimental Medicine · doi:10.1084/jem.150.1.117 · Cited by 49 · cited 3× · see citing works
“The second non-neurotropic virus belonged to the H3N2 subtype, maHK68 (mouse-adapted A/Hong-Kong/1/68) (Haller et al., 1979).”
BackgroundInfluentialBordner, K. A., Kitchen, R. R., Carlyle, B. C., George, E. D., Mahajan, M. C., Mane, S., Taylor, J. R., & Simen, A. A. (2011) · Experimental Gerontology · doi:10.1016/j.exger.2011.03.003 · Cited by 41 · cited 1× · see citing works
“It is interesting that the interferon-responsive gene Ifit3, which is reported to be involved in cognitive decline in aged mice (Bordner et al., 2011), was specifically upregulated in the hippocampus of H7N7-infected mice and is mainly expressed in granule cells (Cho et al.”
BackgroundElmore, M. R. P., Burton, M. D., Conrad, M. S., Rytych, J. L., Alstine, W. G. V., & Johnson, R. W. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2180-13.2014 · Cited by 41 · cited 1× · see citing works
“, IL-1 , IL-6, TNF- , and IFN- ) can be observed across multiple brain regions, including the hippocampus (Howe et al., 2012; Elmore et al., 2014; Heneka et al., 2014; Klein et al., 2017).”
BackgroundGerhauser, I., Alldinger, S., & Baumgärtner, W. (2007) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2007.05.019 · Cited by 39 · cited 1× · see citing works
“In addition, immunohistochemistry for the virus was analyzed using a semiquantitative scoring system from 0 no, 1 few, 2 multiple, to 3 numerous infected cells (Gerhauser et al., 2007).”
MethodSelf-citationAvian influenza and the brain—Comments on the occasion of resurrection of the Spanish flu virus
Kristensson, K. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.11.022 · Cited by 38 · cited 1× · see citing works
“For instance, the highly pathogenic avian influenza virus (H5N1) can infect the CNS and subsequently lead to neuronal cell death in the substantia nigra pars compacta (Kristensson, 2006; Jang et al., 2012) induced by neuroinflammation through the activation of glial cells and altered proinflammatory/inflammatory cytok…”
BackgroundHoyo-Becerra, C., Liu, Z., Yao, J., Kaltwasser, B., Gerken, G., Hermann, D. M., & Schlaak, J. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8861-z · Cited by 37 · see citing works
DiOrio, M., de Fijter, S., Schwartz, M., Page, S. L., Jhung, M. A., Finelli, L., Peacock, G., Yeung, L. F., Honein, M. A., Moore, C. A., et al. (2012) · Cited by 27 · see citing works
The Mouse as Model System to Study Host‐Pathogen Interactions in Influenza A Infections
Wilk, E., & Schughart, K. (2012) · Current Protocols in Mouse Biology · doi:10.1002/9780470942390.mo110173 · Cited by 22 · see citing works
Self-citationNeurologic Complications of Influenza
Shah, S., Keil, A. D., Gara, K. L., & Nagarajan, L. (2013) · Journal of Child Neurology · doi:10.1177/0883073813499610 · Cited by 21 · cited 1× · see citing works
“However, evidence accumulates that an infection with IAV may also be associated with neurological complications in humans (Surana et al., 2011; Ekstrand, 2012; Shah et al., 2014).”
BackgroundHodgson, N. R., Bohnet, S. G., Majde, J. A., & Krueger, J. M. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.07.238 · Cited by 18 · cited 2× · see citing works
“First, we used the well characterized PR8 (A/PuertoRico/8/34) nonneurotropic virus (Majde et al., 2007; Hodgson et al., 2012).”
BackgroundMethodShinya, K., Suto, A., Kawakami, M., Sakamoto, H., Umemura, T., Kawaoka, Y., Kasai, N., & Ito, T. (2005) · Archives of Virology · doi:10.1007/s00705-005-0539-4 · Cited by 18 · cited 1× · see citing works
“Avian H7N7 viruses are able to infect humans and represent a potential future pandemic threat (Lang et al., 1981; Banks et al., 1998; Fouchier et al., 2004; Shinya et al., 2005).”
BackgroundWhishaw, I. Q. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.04.011 · Cited by 17 · see citing works
Sinanan, K., & Hillary, I. B. (1981) · The British Journal of Psychiatry · doi:10.1192/bjp.138.2.131 · Cited by 16 · cited 1× · see citing works
“Interestingly, the dopamine neurotransmitter transporter gene Slc6a3, which has been associated with depression and other neuropsychiatric disorders (Sinanan and Hillary, 1981; Uddin et al., 2011), was among the most strongly upregulated genes especially after H7N7 infection.”
BackgroundWhishaw, I. Q. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.04.013 · Cited by 13 · see citing works
Cellular Antiviral Factors that Target Particle Infectivity of HIV-1
Goffinet, C. (2016) · Current HIV Research · doi:10.2174/1570162x14666151216145521 · Cited by 13 · see citing works
Dynamic gene expression analysis in a H1N1 influenza virus mouse pneumonia model
Bao, Y., Gao, Y., Shi, Y., & Cui, X. (2017) · Virus Genes · doi:10.1007/s11262-017-1438-y · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Desforges, M., Le Coupanec, A., Dubeau, P., Bourgouin, A., Lajoie, L., Dubé, M., & Talbot, P. J. (2019) · Viruses · doi:10.3390/v12010014 · Cited by 1,048 · see citing works
“Animal models have shown that, using either the olfactory route or vagus nerve, influenza A virus may have access to the CNS and alter the hippocampus and the regulation of neurotransmission, while affecting cognition and behavior as long-term sequelae [8, 69, [159] [160] [161] [162] .”
BackgroundNeurologic alterations due to respiratory virus infections
Bohmwald, K., Gálvez, N. M. S., Ríos, M., & Kalergis, A. M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00386 · Cited by 636 · see citing works
“According to these findings, specifically the detection of the viral RNA in the hippocampus, Hosseini et al. (2018) recently evaluated three different mouse-adapted IAVs: two non-neurotropic virus H1N1 (PR8) and H3N2 (maHK68); one neurotropic virus H7N7 (rSC35M).”
BackgroundInfluentialDysregulation of brain and choroid plexus cell types in severe COVID-19
Yang, A. C., Kern, F., Losada, P. M., Agam, M. R., Maat, C. A., Schmartz, G. P., Fehlmann, T., Stein, J. A., Schaum, N., Lee, D. P., et al. (2021) · Nature · doi:10.1038/s41586-021-03710-0 · Cited by 620 · see citing works
Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation
Fernández-Castañeda, A., Lu, P., Geraghty, A. C., Song, E., Lee, M.-H., Wood, J., O’Dea, M. R., Dutton, S., Shamardani, K., Nwangwu, K., et al. (2022) · Cell · doi:10.1016/j.cell.2022.06.008 · Cited by 521 · see citing works
The neurobiology of long COVID
Monje, M., & Iwasaki, A. (2022) · Neuron · doi:10.1016/j.neuron.2022.10.006 · Cited by 415 · see citing works
“The similarities and differences evident between influenza—a disease also associated with neurological and neuropsychiatric sequalae (Honigsbaum 2013; Hosseini et al., 2018; Jurgens et al., 2012; Menninger, 1919)—and SARS-CoV-2 infections underscore the principle that the immune response to a…”
Yachou, Y., Idrissi, A. E., Belapasov, V., & BenAli, S. A. (2020) · Neurological Sciences · doi:10.1007/s10072-020-04575-3 · Cited by 374 · see citing works
Lonnemann, N., Hosseini, S., Marchetti, C., Skouras, D. B., Stefanoni, D., D’Alessandro, A., Dinarello, C. A., & Korte, M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2009680117 · Cited by 298 · see citing works
“5, LIN) (72, 73).”
Self-citationLi, Z., Liu, T., Yang, N., Han, D., Mi, X., Li, Y., Liu, K., Vuylsteke, A., Xiang, H., & Guo, X. (2020) · Frontiers of Medicine · doi:10.1007/s11684-020-0786-5 · Cited by 267 · see citing works
“Influenza A virus may have access to the CNS and alter the hippocampus function via the vagus nerve, affecting cognition and behavior [53, 54] .”
BackgroundMontani, D., Savale, L., Noël, N., Meyrignac, O., Colle, R., Gasnier, M., Corruble, E., Beurnier, A., Jutant, E., Pham, T. O., et al. (2022) · European Respiratory Review · doi:10.1183/16000617.0185-2021 · Cited by 266 · see citing works
The cognitive consequences of the COVID-19 epidemic: collateral damage?
Ritchie, K., Chan, D., & Watermeyer, T. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa069 · Cited by 226 · see citing works
Alonso-Lana, S., Marquié, M., Ruiz, A., & Boada, M. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.588872 · Cited by 207 · see citing works
Cerebral dysfunctions caused by sepsis during ageing
Manabe, T., & Heneka, M. T. (2022) · Nature Reviews Immunology · doi:10.1038/s41577-021-00643-7 · Cited by 191 · see citing works
Unraveling the Possible Routes of SARS-COV-2 Invasion into the Central Nervous System
Lima, M., Siokas, V., Aloizou, A., Liampas, I., Mentis, A. A., Tsouris, Z., Papadimitriou, A., Mitsias, P. D., Tsatsakis, A. M., Bogdanos, D. P., et al. (2020) · Current Treatment Options in Neurology · doi:10.1007/s11940-020-00647-z · Cited by 126 · see citing works
Microglia at the blood brain barrier in health and disease
Mayer, M. G., & Fischer, T. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1360195 · Cited by 128 · see citing works
Infectious disease-associated encephalopathies
Barbosa‐Silva, M. C., Lima, M. N., Battaglini, D., Robba, C., Pelosi, P. P., Rocco, P. R. M., & Maron‐Gutierrez, T. (2021) · Critical Care · doi:10.1186/s13054-021-03659-6 · Cited by 120 · see citing works
Infection and Risk of Parkinson’s Disease
Smeyne, R. J., Noyce, A. J., Byrne, M., Savica, R., & Marras, C. (2021) · Journal of Parkinson's Disease · doi:10.3233/jpd-202279 · Cited by 125 · see citing works
“[16], the 1968 H3N2 (Hong Kong flu) [17] and the”
BackgroundBukhbinder, A. S., Ling, Y., Hasan, O., Jiang, X., Kim, Y., Phelps, K. N., Schmandt, R. E., Amran, A., Coburn, R. P., Ramesh, S., et al. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-220361 · Cited by 106 · see citing works
“An association between flu infection and AD risk is supported by mouse studies demonstrating that peripheral infection of wild-type mice with non-neurotropic influenza strains induces excessive microglial activation and subsequent alteration of neuronal morphology, particularly in the hippocampus, that persists after…”
BackgroundFernández-Castañeda, A., Lu, P., Geraghty, A. C., Song, E., Lee, M.-H., Wood, J., Yalçın, B., Taylor, K. R., Dutton, S., Acosta-Alvarez, L., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.07.475453 · Cited by 101 · see citing works
Damiano, R. F., Guedes, B. F., de Rocca, C. C., de Pádua Serafim, A., Castro, L. H. M., Munhoz, C. D., Nitrini, R., Filho, G. B., Miguel, E. C., Lucchetti, G., et al. (2022) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-021-01286-4 · Cited by 98 · see citing works
Long-Term Outcomes of Pediatric Infections: From Traditional Infectious Diseases to Long Covid
Buonsenso, D., Gennaro, L. D., Rose, C. D., Morello, R., D’Ilario, F., Zampino, G., Piazza, M., Boner, A. L., Iraci, C., O’Connell, S., et al. (2022) · Future Microbiology · doi:10.2217/fmb-2022-0031 · Cited by 91 · see citing works
Proal, A. D., & Marshall, T. G. (2018) · Frontiers in Pediatrics · doi:10.3389/fped.2018.00373 · Cited by 77 · see citing works
“Another study found that, up to a month after initial infection, influenza viruses regulated the long-term expression of inflammatory and neuron/glia-specific genes in mice (142).”
BackgroundEffect of Systemic Inflammation in the CNS: A Silent History of Neuronal Damage
Solano, M. V. M., Lara, C. S., Sánchez-Garibay, C., Soto-Rojas, L. O., Escobedo-Ávila, I., Tena‐Suck, M. L., Ortiz-Butrón, R., Choreño-Parra, J. A., Romero‐López, J. P., & Meléndez-Camargo, M. E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241511902 · Cited by 77 · see citing works
“On the other hand, in murine sepsis studies, it has been shown that there are alterations in cognitive functions related to long-term memory [67,149,162,166,167].”
BackgroundKerr, F., Bjedov, I., & Sofola-Adesakin, O. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00297 · Cited by 78 · see citing works
Hosseini, S., Michaelsen‐Preusse, K., Grigoryan, G., Chhatbar, C., Kalinke, U., & Körte, M. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107666 · Cited by 71 · see citing works
“The hippocampus is a highly plastic brain region, involved in learning and memory formation, which are especially sensitive to cytokines (Hosseini et al., 2018; Korte and Schmitz, 2016).”
BackgroundSelf-citationThe Causes and Long-Term Consequences of Viral Encephalitis
Böhmwald, K., Andrade, C. A., Gálvez, N. M. S., Mora, V. P., Muñóz, J. T., & Kalergis, A. M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.755875 · Cited by 73 · see citing works
“Infection with neurotropic and non-neurotropic Influenza viruses may promote several neurologic sequelae, such as cognitive impairment, anxiety behavior, learning difficulties, and memory problems, as studies performed on mice have demonstrated (Hosseini et al., 2018).”
BackgroundThe impact of neuroinflammation on neuronal integrity
Tastan, B., & Heneka, M. T. (2024) · Immunological Reviews · doi:10.1111/imr.13419 · Cited by 77 · see citing works
“…resulting from viral infections can have profound consequences on the CNS. Viral infections caused by common viruses such as Influenza, 90,91 Herpes simplex virus, 92 Zika virus, 93 Corona Virus, 94 human immunodeficiency virus, 95 or hepatitis C, 96 Streptococcus triggered an…”
Düsedau, H. P., Steffen, J., Figueiredo, C. A., Boehme, J. D., Schultz, K., Erck, C., Körte, M., Faber‐Zuschratter, H., Smalla, K., Dieterich, D. C., et al. (2021) · mBio · doi:10.1128/mbio.01776-21 · Cited by 69 · see citing works
Neuroinflammation in neurodegeneration via microbial infections
Tran, V. T. A., Lee, L. P., & Cho, H. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.907804 · Cited by 68 · see citing works
The Communication Between the Immune and Nervous Systems: The Role of IL-1β in Synaptopathies
Pozzi, D., Menna, E., Canzi, A., Desiato, G., Mantovani, C., & Matteoli, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00111 · Cited by 63 · see citing works
“As an example, influenza infection associated to elevated pro-inflammatory cytokines was found to alter neuronal morphology leading to cognitive impairment in adult mice (Jurgens et al., 2012; Hosseini et al., 2018).”
BackgroundRizzo, M. D., Crawford, R. B., Bach, A. P., Sermet, S., Amalfitano, A., & Kaminski, N. E. (2019) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.119.260661 · Cited by 61 · see citing works
“Furthermore, because influenza has been identified in the brain and induces neuroinflammation (Jurgens et al., 2012; Hosseini et al., 2018), the immune-suppressive effects of THC observed heremight also be detrimental to host defense against this virus.”
BackgroundMoghaddam, B. F., & Fereidoni, M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0229769 · Cited by 61 · see citing works
“This test needs cognitive flexibility [65].”
Acıoğlu, Ç., & Elkabes, S. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03360-3 · Cited by 64 · see citing works
The Influence of Virus Infection on Microglia and Accelerated Brain Aging
Filgueira, L., Larionov, A. A., & Lannes, N. (2021) · Cells · doi:10.3390/cells10071836 · Cited by 57 · see citing works
“Neurons, astrocytes, endothelial cells Experimental animal studies [176,177] Neurotoxicity, neuroinflammation, break-down of blood-brain barrier Encephalitis”
BackgroundMicroglial Priming in Infections and Its Risk to Neurodegenerative Diseases
Lima, M. N., Barbosa‐Silva, M. C., & Maron‐Gutierrez, T. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.878987 · Cited by 57 · see citing works
Disruption of the Blood-Brain Barrier During Neuroinflammatory and Neuroinfectious Diseases
Salimi, H., & Klein, R. S. (2019) · Contemporary clinical neuroscience · doi:10.1007/978-3-030-19515-1_7 · Cited by 54 · see citing works
Bączyńska, E., Pels, K. K., Basu, S., Włodarczyk, J., & Ruszczycki, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084053 · Cited by 47 · see citing works
“Influenza infection Hosseini et al. 2018 J. Neurosci.”
BackgroundTherapeutic Role of Inflammasome Inhibitors in Neurodegenerative Disorders
Lahooti, B., Chhibber, T., Bagchi, S., Varahachalam, S. P., & Jayant, R. D. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.11.004 · Cited by 50 · see citing works
Neurological Damage by Coronaviruses: A Catastrophe in the Queue!
Mishra, R., & Banerjea, A. C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.565521 · Cited by 49 · see citing works
Dolatshahi, M., Sabahi, M., & Aarabi, M. H. (2021) · Molecular Neurobiology · doi:10.1007/s12035-020-02236-2 · Cited by 49 · see citing works
The cognitive and psychiatric subacute impairment in severe Covid-19
Serrano-Castro, P. J., Garzón-Maldonado, F. J., Naranjo, I. C., Ollero-Ortiz, A., Mínguez‐Castellanos, A., Iglesias-Espinosa, M., Baena-Palomino, P., Sánchez, V. S., Pérez, R. M. S., Rubi-Callejon, J., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-07559-9 · Cited by 49 · see citing works
Bauer, L., Benavides, F. F. W., Kroeze, E. J. B. V., de Wit, E., & van Riel, D. A. J. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.08.002 · Cited by 49 · see citing works
“Additionally, influenza A virus infections can disturb the brain homeostasis through alterations in hippocampal neuron morphology and neuronal connectivity [91].”
Environmental Signals on Microglial Function during Brain Development, Neuroplasticity, and Disease
Chagas, L. D. S., Sandre, P. C., Ribeiro, N. C. A. R. E., Marcondes, H., Silva, P. O., Savino, W., & Serfaty, C. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062111 · Cited by 50 · see citing works
“In this work, it was also demonstrated that the loss of hippocampal dendritic spines caused by the virus persists beyond the acute phase of infection and is directly associated with the increase in the number of activated microglia, reduction of the hippocampal long-term potentiation (LTP), and the resulting deficits…”
Backgroundde Paula, J. J., de Paiva, R. E. R. P., Silva, N. G. S. E., Rosa, D. V., Duran, F., Coimbra, R. S., Costa, D. D. S., Dutenhefner, P. R., Oliveira, H. S. D., Camargos, S., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01632-5 · Cited by 49 · see citing works
“In infections with influenza A virus (IAV), neuropsychiatric complications were reported after infection with either neurotropic or non-neurotropic variants [48], suggesting that viral infections can provoke neuroinflammation via peripherallyproduced cytokines.”
BackgroundHosseini, S., Michaelsen‐Preusse, K., Schughart, K., & Körte, M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.643650 · Cited by 46 · see citing works
Self-citationThe transcriptomic profiling of SARS-CoV-2 compared to SARS, MERS, EBOV, and H1N1
Alsamman, A. M., & Zayed, H. (2020) · PLoS ONE · doi:10.1371/journal.pone.0243270 · Cited by 46 · see citing works
“Significant NRCAM gene expression has been observed under specific circumstances, such as neuroinflammation triggered by influenza A long-term viral infection [51].”
BackgroundBircak-Kuchtova, B., Chung, H., Wickel, J., Ehler, J., & Geis, C. (2023) · Critical Care · doi:10.1186/s13054-023-04497-4 · Cited by 46 · see citing works
Böhmwald, K., Soto, J. A., Andrade, C. A., Fernández‐Fierro, A., Espinoza, J. A., Ríos, M., Eugenín, E. A., González, P. A., Opazo, M. C., Riedel, C. A., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.09.021 · Cited by 43 · see citing works
“It has been observed an increase in the BBB permeability in mice infected with influenza virus (Hosseini et al., 2018).”
NLRP3 and Infections: β-Amyloid in Inflammasome beyond Neurodegeneration
Sita, G., Graziosi, A., Hrelia, P., & Morroni, F. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136984 · Cited by 42 · see citing works
“Indeed, several respiratory virus infections have been shown to propagate in cerebral regions associated with learning and cognitive abilities [104].”
BackgroundSiegers, J. Y., van de Bildt, M. W. G., Lin, Z., Leijten, L. M., Lavrijssen, R. A. M., Bestebroer, T., Spronken, M. I. J., De Zeeuw, C. I., Gao, Z., Schrauwen, E. J. A., et al. (2019) · Journal of Virology · doi:10.1128/jvi.02273-18 · Cited by 40 · see citing works
Boscolo‐Rizzo, P., Hummel, T. R., Invitto, S., Spinato, G., Tomasoni, M., Emanuelli, E., Tofanelli, M., Cavicchia, A., Grill, V., Vaira, L. A., et al. (2023) · International Forum of Allergy & Rhinology · doi:10.1002/alr.23148 · Cited by 41 · see citing works
“49 Thus, the present findings, in addition to describing the long-term prevalence and recovery rates of smell and taste impairment in subjects who were affected by mild to moderate forms of COVID-19, mirror what has been observed in patients affected by long COVID-19 dominated by the so-called…”
ResultSepsis-Associated Encephalopathy: A Mini-Review of Inflammation in the Brain and Body
Ito, H., Hosomi, S., Koyama, Y., Matsumoto, H., Imamura, Y., Ogura, H., & Oda, J. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.912866 · Cited by 40 · see citing works
Lee, J. C., Nallani, R., Cass, L., Bhalla, V., Chiu, A. G., & Villwock, J. A. (2020) · American Journal of Rhinology and Allergy · doi:10.1177/1945892420957853 · Cited by 39 · see citing works
Investigating the potential mechanisms of depression induced-by COVID-19 infection in patients
Mohammadkhanizadeh, A., & Nikbakht, F. (2021) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2021.07.023 · Cited by 37 · see citing works
“The specific vulnerability of the hippocampus to other respiratory virus infections, like the influenza virus, has been previously observed in mice [53].”
BackgroundSARS-CoV-2-Mediated Neuropathogenesis, Deterioration of Hippocampal Neurogenesis and Dementia
Radhakrishnan, R. K., & Kandasamy, M. (2022) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/15333175221078418 · Cited by 35 · see citing works
León‐Rodríguez, A., Fernández‐Arjona, M. D. M., Grondona, J. M., Pedraza, C., & López-Ávalos, M. D. (2022) · Scientific Reports · doi:10.1038/s41598-022-15617-5 · Cited by 37 · see citing works
Wongchitrat, P., Shukla, M., Sharma, R., Govitrapong, P., & Reiter, R. J. (2021) · Antioxidants · doi:10.3390/antiox10010047 · Cited by 35 · see citing works
“Conversely, the H1N1 flu strain is not capable of crossing the BBB, but still can cause the CNS immune cells to invade the substantia nigra and the hippocampus, causing inflammation and cell death in those areas [67,68].”
BackgroundMolecular Mechanisms in the Genesis of Seizures and Epilepsy Associated With Viral Infection
Löscher, W., & Howe, C. L. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.870868 · Cited by 33 · see citing works
Wu, K.-C., Lee, C.-Y., Chou, F.-Y., Chern, Y., & Lin, C. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.11.008 · Cited by 34 · see citing works
Ohm, M., Hosseini, S., Lonnemann, N., He, W., More, T. H., Goldmann, O., Medina, E., Hiller, K., & Körte, M. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03188-3 · Cited by 33 · see citing works
“Neuroinflam-mation can eventually impair cognitive functions such as learning and memory processes well beyond the initial phase of sepsis or viral infection [6, 29].”
BackgroundMethodSelf-citationНиколаевна, Б. А., Pershin, V. I., Zaborskaya, O. G., Tkachenko, N., Mironov, A. A., Guryev, E. L., Kurbatov, L. K., Gainullin, M., & Mukhina, I. V. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01033 · Cited by 32 · see citing works
“This finding correlates with the previously made by Hosseini et al. (2018) where the overexpression of inflammatory factors didn’t affect the activity of animals in open field test, although the chronic inflammation can lead to a memory loss (Zhou et al., 2016).”
ResultCOVID-19 and Neurodegenerative Diseases: Prion-Like Spread and Long-Term Consequences
Baazaoui, N., & Iqbal, K. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-220105 · Cited by 32 · see citing works
“deterioration in the hippocampus-dependent learning 533 and a reduction in the long-term potentiation asso534 ciated impairment in spatial memory were reported 535 [110].”
BackgroundCamp, B., Stegemann‐Koniszewski, S., & Schreiber, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115699 · Cited by 31 · see citing works
“Furthermore, persisting neuro-inflammation has been observed following infection with neurotropic as well as non-neurotropic IAV strains in mice [110].”
BackgroundSerafini, R. A., Frere, J. J., Zimering, J. H., Giosan, I. M., Pryce, K. D., Golynker, I., Panis, M., Ruiz, A., tenOever, B. R., & Zachariou, V. (2023) · Science Signaling · doi:10.1126/scisignal.ade4984 · Cited by 30 · see citing works
“In these studies, the source of coronavirus-induced neurological dysfunction was linked to two major causes: direct virus-induced damage and collateral damage to host cells by antiviral immune responses (48, 49).”
BackgroundPiacentini, R., & Grassi, C. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-23-01690 · Cited by 30 · see citing works
“Noteworthy, other than pulmonary diseases, infection by influenza viruses induces had been reported to induce cognitive deficit and synaptic remodeling associated with increased pro-inflammatory cytokines (IL-1β, IL-6, TNF-α, IFN-α) (Jurgens et al., 2012; Hosseini et al., 2018).”
BackgroundCiticoline and COVID-19-Related Cognitive and Other Neurologic Complications
Turana, Y., Nathaniel, M., Shen, R., Ali, S., & Aparasu, R. R. (2021) · Brain Sciences · doi:10.3390/brainsci12010059 · Cited by 33 · see citing works
Zhang‐James, Y., Clay, J. W. S., Aber, R. B., Gamble, H. M., & Faraone, S. V. (2024) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2024.03.023 · Cited by 28 · see citing works
Lonnemann, N., Hosseini, S., Ohm, M., Geffers, R., Hiller, K., Dinarello, C. A., & Körte, M. (2022) · eLife · doi:10.7554/elife.75889 · Cited by 28 · see citing works
Self-citationPlasmalogens inhibit neuroinflammation and promote cognitive function
Hossain, M. S., Mawatari, S., & Fujino, T. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.11.005 · Cited by 28 · see citing works
Neurotrophin Signaling Impairment by Viral Infections in the Central Nervous System
Böhmwald, K., Andrade, C. A., Mora, V. P., Muñóz, J. T., Ramírez, R. A., Rojas, M. F., & Kalergis, A. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105817 · Cited by 27 · see citing works
“Interestingly, in vivo studies have demonstrated that the levels of BDNF decrease in the hippocampus of influenza virus-infected mice, regardless of whether they are neurotropic (H3N2 and H7N7) or non-neurotropic (H1N1) [142,143].”
BackgroundGrant, R. A., Poor, T. A., Sichizya, L., Diaz, E., Bailey, J. I., Soni, S., Senkow, K. J., Pérez-Leonor, X. G., Abdala‐Valencia, H., Lu, Z., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.178859 · Cited by 27 · see citing works
“Nevertheless, prolonged cognitive dysfunction in survivors of pneumonia or sepsis was recognized before the pandemic (4, 7–9 , 23– 26).”
BackgroundOrchestration of antiviral responses within the infected central nervous system
Pavlou, A., Mulenge, F., Gern, O. L., Busker, L. M., Greimel, E., Waltl, I., & Kalinke, U. (2024) · Cellular and Molecular Immunology · doi:10.1038/s41423-024-01181-7 · Cited by 24 · see citing works
Cornelius, A., Hosseini, S., Schreier, S., Fritzsch, D., Weichert, L., Michaelsen‐Preusse, K., Fendt, M., & Kröger, A. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01951-w · Cited by 24 · see citing works
“Other studies show that this effect was not limited to acute infection and lasts longer [20].”
BackgroundMethodInfluentialSelf-citationBöhmwald, K., Andrade, C. A., & Kalergis, A. M. (2021) · Pharmaceuticals · doi:10.3390/ph14040340 · Cited by 28 · see citing works
Petrisko, T. J., Gómez-Arboledas, Á., & Tenner, A. J. (2021) · Advances in immunology · doi:10.1016/bs.ai.2021.09.003 · Cited by 22 · see citing works
Biological agents and the aging brain: glial inflammation and neurotoxic signaling
Latham, A. S., Moreno, J. A., & Geer, C. E. (2023) · Frontiers in Aging · doi:10.3389/fragi.2023.1244149 · Cited by 25 · see citing works
“Interestingly, these long-term CNS alterations occurred in non-neurotropic strains of the virus as well (Hosseini et al., 2018).”
BackgroundThe Impact of Non-Neurotropic Influenza Strains on the Brain: A Role for Microglial Priming?
Barbosa‐Silva, M. C., Santos, L. E., & Rangel, B. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1368-18.2018 · Cited by 23 · see citing works
“Despite the eventual recovery, the central effects observed by Hosseini et al. (2018) might have long-term consequences, due to innate immune plasticity.”
BackgroundMethodResultInfluentialKarthik, S., Saraswathi, I., Alarifi, A., Al-Atram, A. A., Mickeymaray, S., Paramasivam, A., Shaikh, S., Jeraud, M., & Alothaim, A. S. (2022) · PeerJ · doi:10.7717/peerj.14227 · Cited by 23 · see citing works
Mayer, M. G., & Fischer, T. (2025) · American Journal Of Pathology · doi:10.1016/j.ajpath.2025.03.011 · Cited by 21 · see citing works
Neuroinflammation in Post COVID‐19 Sequelae: Neuroinvasion and Neuroimmune Crosstalk
Reis, R. S. D., Selvam, S., & Ayyavoo, V. (2024) · Reviews in Medical Virology · doi:10.1002/rmv.70009 · Cited by 20 · see citing works
Mathematical Model Shows How Sleep May Affect Amyloid-β Fibrillization
Hoore, M., Khailaie, S., Montaseri, G., Mitra, T., & Meyer‐Hermann, M. (2020) · Biophysical Journal · doi:10.1016/j.bpj.2020.07.011 · Cited by 20 · see citing works
Radzišauskienė, D., Vitkauskaitė, M., Žvinytė, K., & Mameniškienė, R. (2020) · Brain and Behavior · doi:10.1002/brb3.1916 · Cited by 20 · see citing works
Rizzo, M. D., Crawford, R. B., Bach, A. P., Sermet, S., Amalfitano, A., & Kaminski, N. E. (2019) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2019.576969 · Cited by 19 · see citing works
Froggatt, H. M., & Heaton, N. S. (2022) · FEBS Journal · doi:10.1111/febs.16363 · Cited by 20 · see citing works
Long-term Consequences of COVID-19: Chemosensory Disorders
Liao, B., Deng, Y., Zeng, M., & Liu, Z. (2022) · Current Allergy and Asthma Reports · doi:10.1007/s11882-022-01062-x · Cited by 18 · see citing works
Influenza vaccine is able to prevent neuroinflammation triggered by H7N7 IAV infection
Demuth, L., Ohm, M., Michaelsen‐Preusse, K., Schulze, K., Riese, P., Guzmán, C. A., Körte, M., & Hosseini, S. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1142639 · Cited by 17 · see citing works
“Experiments in animal models have previously shown that IAV infections trigger neuroinflammation in the acute phase of the disease, including activation of microglia and release of proinflammatory cytokines (Jang et al., 2012; Jurgens et al., 2012; Sadasivan et al., 2015; Hosseini et al., 2018).”
BackgroundMethodInfluentialSelf-citationClark, J. J., Penrice-Randal, R., Sharma, P., Dong, X., Pennington, S. H., Marriott, A. E., Colombo, S. A. P., Davidson, A. D., Williamson, M. K., Matthews, D. A., et al. (2024) · Viruses · doi:10.3390/v16060863 · Cited by 18 · see citing works
“While brain infection has been well documented in cases of influenza [53–55], this is predominantly limited to neurotropic and highly pathogenic strains and occurs via the breakdown of the BBB following high levels of viremia [54,56].”
BackgroundUnaltered T cell responses to common antigens in individuals with Parkinson's disease
Williams, G. P., Muskat, K., Frazier, A., Xu, Y., Mateus, J., Grifoni, A., Antunes, R. D. S., Weiskopf, D., Amara, A. W., Standaert, D. G., et al. (2022) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2022.120510 · Cited by 17 · see citing works
Al-Shalan, H. A. M., Lü, Z., Dong, Z., Wang, P., Nicholls, P. K., Boughton, B. A., Stumbles, P. A., Greene, W. K., & Ma, B. (2023) · Virology Journal · doi:10.1186/s12985-023-02239-0 · Cited by 17 · see citing works
“…which IAV causes acute and long-term primary/ secondary neuroinflammatory/neurological disorders/ complications (e.g., seizures, encephalopathy, brain fog, encephalitis, stroke, focal neurologic deficits, Guillain-Barré syndrome, acute disseminated encephalomyelitis, and transverse myelitis) [44].”
BackgroundLiang, L., Mao, S., Wang, J., Ding, X., & Zen, J. (2019) · ExRNA · doi:10.1186/s41544-019-0031-z · Cited by 16 · see citing works
“Infection by neurotropic viruses as well as the consequent immune response can lead to irreversible disruption of functional structure in CNS, which frequently cause significant clinical phenotype [21, 22, 60].”
BackgroundRole of Necroptosis in Central Nervous System Diseases
Shao, H., Wu, W., Wang, P., Han, T., & Zhuang, C. (2022) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.2c00405 · Cited by 16 · see citing works
Clark, J. J., Penrice-Randal, R., Sharma, P., Kipar, A., Dong, X., Pennington, S. H., Marriott, A. E., Colombo, S. A. P., Davidson, A. D., Williamson, M. K., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.13.334532 · Cited by 17 · see citing works
How viral infections cause neuronal dysfunction: a focus on the role of microglia and astrocytes
Hosseini, S., & Korte, M. (2023) · Biochemical Society Transactions · doi:10.1042/bst20220771 · Cited by 17 · see citing works
Self-citationSaucier, J., Comeau, D., Robichaud, G. A., & Chamard-Witkowski, L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1221266 · Cited by 16 · see citing works
“These processes alter BBB permeability, structural hippocampal plasticity, and may underlie cognitive dysfunction (86, 87).”
BackgroundViral infection and host immune response in diabetes
Joshi, G., Das, A., Verma, G., & Guchhait, P. (2023) · IUBMB Life · doi:10.1002/iub.2794 · Cited by 16 · see citing works
Chen, H., Lan, S., Tseng, Y., Chang, Y., Lu, Y., & Lan, M. (2024) · BMC Infectious Diseases · doi:10.1186/s12879-024-09844-6 · Cited by 15 · see citing works
“This mechanism has been shown to contribute to the neurological complications associated with nonneurotropic influenza strains, such as H1N1 [51] and H3N2 [52].”
BackgroundWang, B., Su, Q., Luo, J., Li, M., Wu, Q., Chang, H., Du, J., Huang, C., Ma, J., Han, S., et al. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.593202 · Cited by 15 · see citing works
Cassidy, B. R., Sonntag, W. E., Leenen, P. J. M., & Drevets, D. A. (2022) · Immunity & Ageing · doi:10.1186/s12979-022-00281-0 · Cited by 14 · see citing works
The microbiome in post-acute infection syndrome (PAIS)
Guo, C., Yi, B., Wu, J., & Lu, J. (2023) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2023.08.002 · Cited by 14 · see citing works
“glia in mice up to a month after the initial infection [57].”
BackgroundSieracka, J., Sieracki, P., Kozera, G., Szurowska, E., Gulczyński, J., Sobolewski, P. K., Kloc, W., & Iżycka‐Świeszewska, E. (2021) · Folia Neuropathologica · doi:10.5114/fn.2021.105128 · Cited by 14 · see citing works
“Common non-neurotrophic strains of influenza can cause injury to the hippocampus, interfering with normal behaviour after the acute infection [43].”
BackgroundA Cytokine-based model for the pathophysiology of Long COVID symptomsPreprint
Low, R. N., Low, R. J., & Akrami, A. (2020) · doi:10.31219/osf.io/7gcnv · Cited by 14 · see citing works
- Authors
- Hosseini, S., Wilk, E., Michaelsen-Preusse, K., Gerhauser, I., Baumgärtner, W., Geffers, R., Schughart, K., & Korte, M.
- Affiliations
- Helmholtz Centre for Infection Research (DE)
- University of Veterinary Medicine Hannover, Foundation (DE)
- University of Tennessee Health Science Center (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-02-27
- Volume
- 38
- Issue
- 12
- Pages
- 3060-3080
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6596076
- OpenAlex
- W2788200071
- Cited by
- 236
- References
- 101
- Citations by year
- 2026: 26 · 2025: 31 · 2024: 36 · 2023: 37 · 2022: 37 · 2021: 31 · 2020: 25 · 2019: 8 · 2018: 5
- FWCI
- 7.74
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digitale Bibliothek Braunschweig (Verbundzentrale Göttingen (VZG)) (submittedVersion)
- HZI (Helmholtz Centre for Infection Research) (submittedVersion, cc-by-nc-sa)
- LeoPARD - TU Braunschweig Publications And Research Data
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Infectious Diseases › Infectious Encephalopathies and Encephalitis
- Keywords
- influenza A virus, neuroinflammation, hippocampus, dendritic spine loss, H7N7, H3N2, H1N1, microglial activation, long-term potentiation, spatial memory impairment, neuronal morphology, transcriptome, cognitive impairment, viral encephalitis
- MeSH terms
- Animals, Female, Hippocampus, Inflammation, Mice, Inbred C57BL, Orthomyxoviridae Infections, Dendritic Spines, Mice, Influenza A Virus, H1N1 Subtype, Influenza A Virus, H3N2 Subtype, Influenza A Virus, H7N7 Subtype
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