Coronavirus Neurovirulence Correlates with the Ability of the Virus To Induce Proinflammatory Cytokine Signals from Astrocytes and Microglia
Open accessAbstract
The molecular and cellular basis of coronavirus neurovirulence is poorly understood. Since neurovirulence may be determined at the early stages of infection of the central nervous system (CNS), we hypothesize that it may depend on the ability of the virus to induce proinflammatory signals from brain cells for the recruitment of blood-derived inflammatory cells. To test this hypothesis, we studied the interaction between coronaviruses (mouse hepatitis virus) of different neurovirulences with primary cell cultures of brain immune cells (astrocytes and microglia) and mouse tissues. We found that the level of neurovirulence of the virus correlates with its differential ability to induce proinflammatory cytokines (interleukin 12 [IL-12] p40, tumor necrosis factor alpha, IL-6, IL-15, and IL-1β) in astrocytes and microglia and in mouse brains and spinal cords. These findings suggest that coronavirus neurovirulence may depend on a novel discriminatory ability of astrocytes and microglia to induce a proinflammatory response in the CNS.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Direct viral neuro-invasion and its association with ACE-2 expression in brain, especially in glial cells, could lead to oxidative stress and neuronal loss, due to microglia and astrocyte activation and increased nitric oxide production.
“Direct viral neuro-invasion, as hypothesized above, and its association with ACE-2 expression in brain, especially in glial cells, could lead to oxidative stress and neuronal loss, due to both microglia and astrocyte activation, and increased nitric oxide (NO) production. [181, 182].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [182]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Mosmann, T. R., Cherwinski, H. M., Bond, M. W., Giedlin, M. A., & Coffman, R. L. (1986) · The Journal of Immunology · doi:10.4049/jimmunol.136.7.2348 · Cited by 7,438 · see citing works
Coronavirus as a possible cause of severe acute respiratory syndrome
Peiris, M. J. S., Lai, S., Poon, L. L. M., Guan, Y., Yam, L., Lim, W., Nicholls, J. M., Yee, W., Yan, W., Cheung, M., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13077-2 · Cited by 2,916 · see citing works
B7-H3: A costimulatory molecule for T cell activation and IFN-γ production
Chapoval, A. I., Ni, J., Lau, J. S., Wilcox, R. A., Flies, D. B., Liu, D., Dong, H., Sica, G., Zhu, G., Tamada, K., et al. (2001) · Nature Immunology · doi:10.1038/85339 · Cited by 1,016 · see citing works
Lieberman, A. P., Pitha, P. M., Shin, H. S., & Shin, M. L. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.16.6348 · Cited by 783 · see citing works
Inflammatory cytokines within the central nervous system: sources, function, and mechanism of action
Benveniste, E. N. (1992) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1992.263.1.c1 · Cited by 608 · see citing works
Sharif, S., Arreaza, G., Zucker, P., Mi, Q., Sondhi, J., Naidenko, O. V., Kronenberg, M., Koezuka, Y., Delovitch, T. L., Gombert, J., et al. (2001) · Nature Medicine · doi:10.1038/nm0901-1057 · Cited by 604 · see citing works
Infection with HIV is associated with elevated IL-6 levels and production.
Breen, E. C., Rezai, A. R., Nakajima, K., Beall, G. N., Mitsuyasu, R. T., Hirano, T., Kishimoto, T., & Martinez-Maza, O. (1990) · The Journal of Immunology · doi:10.4049/jimmunol.144.2.480 · Cited by 578 · see citing works
McInnes, I. B., Leung, B. P. L., Sturrock, R. D., Field, M., & Liew, F. Y. (1997) · Nature Medicine · doi:10.1038/nm0297-189 · Cited by 513 · see citing works
Aloisi, F., Carè, A., Borsellino, G., Gallo, P., Rosa, S., Bassani, A. C. F., Cabibbo, A., Testa, U., Levi, G., & Peschle, C. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.7.2358 · Cited by 400 · see citing works
Pathogenesis of Infectious Disease
(1978) · Postgraduate Medical Journal · doi:10.1136/pgmj.54.627.62-a · Cited by 362 · see citing works
Pathogenesis of demyelination induced by a mouse hepatitis.
Weiner, L. P. (1973) · Archives of Neurology · doi:10.1001/archneur.1973.00490230034003 · Cited by 349 · see citing works
Tada, T., Takemori, T., Okumura, K., Nonaka, M., & Tokuhisa, T. (1978) · The Journal of Experimental Medicine · doi:10.1084/jem.147.2.446 · Cited by 318 · see citing works
Induction of IL-6 (B cell stimulatory factor-2/IFN-beta 2) production by HIV.
Nakajima, K., Martı́nez-Maza, O., Hirano, T., Breen, E. C., Nishanian, P., Salazar-Gonzalez, J. F., Fahey, J. L., & Kishimoto, T. (1989) · The Journal of Immunology · doi:10.4049/jimmunol.142.2.531 · Cited by 304 · see citing works
Siegmund, B., Fantuzzi, G., Rieder, F., Gamboni-Robertson, F., Lehr, H.-A., Hartmann, G., Dinarello, C. A., Endres, S., & Eigler, A. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.4.r1264 · Cited by 289 · see citing works
Okuda, Y., Sakoda, S., Bernard, C. C. A., Fujimura, H., Saeki, Y., Kishimoto, T., & Yanagihara, T. (1998) · International Immunology · doi:10.1093/intimm/10.5.703 · Cited by 244 · see citing works
Microglia in diseases of the central nervous system
Nelson, P. T., Soma, L. A., & Lavi, E. (2002) · Annals of Medicine · doi:10.1080/078538902321117698 · Cited by 222 · see citing works
Self-citationExperimental demyelination produced by the A59 strain of mouse hepatitis virus
Lavi, E., Gilden, D., Wróblewska, Z., Rorke, L., & Weiss, S. (1984) · Neurology · doi:10.1212/wnl.34.5.597 · Cited by 207 · see citing works
Self-citationTsunoda, I., & Fujinami, R. S. (1996) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199606000-00001 · Cited by 184 · see citing works
Olson, J. K., Girvin, A. M., & Miller, S. D. (2001) · Journal of Virology · doi:10.1128/jvi.75.20.9780-9789.2001 · Cited by 178 · see citing works
Chronic central nervous system demyelination in mice after JHM virus infection
Stohlman, S., & Weiner, L. (1981) · Neurology · doi:10.1212/wnl.31.1.38 · Cited by 172 · see citing works
Fa, M., Bauer, S. P., Ak, H., & Winn, W. C. (1973) · PubMed · Cited by 172 · see citing works
Streit, W. J., & Colton, C. A. (1995) · Scientific American · doi:10.1038/scientificamerican1195-54 · Cited by 171 · see citing works
Coronavirus Infection Induces H-2 Antigen Expression on Oligodendrocytes and Astrocytes
Suzumura, A., Lavi, E., Weiss, S. R., & Silberberg, D. H. (1986) · Science · doi:10.1126/science.3010460 · Cited by 171 · see citing works
Self-citationPhillips, J. J., Chua, M. M., Lavi, E., & Weiss, S. R. (1999) · Journal of Virology · doi:10.1128/jvi.73.9.7752-7760.1999 · Cited by 157 · see citing works
Self-citationThe Role of Microglia and Astrocytes in Cns Immune Surveillance and Immunopathology
Aloisi, F. (1999) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4685-6_10 · Cited by 154 · see citing works
Cytokine induction during T-cell-mediated clearance of mouse hepatitis virus from neurons in vivo
Pearce, B. D., Hobbs, M. V., McGraw, T., & Buchmeier, M. J. (1994) · Journal of Virology · doi:10.1128/jvi.68.9.5483-5495.1994 · Cited by 149 · see citing works
Neuron to neuron transmission of herpes simplex virus
Kristensson, K., Nennesmo, I., Persson, L., & Lycke, E. (1982) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(82)90227-1 · Cited by 136 · see citing works
Arend, W. P. (2001) · Seminars in Arthritis and Rheumatism · doi:10.1053/sarh.2001.23693 · Cited by 131 · see citing works
SUN, N., Grzybicki, D. M., Castro, R. F., Murphy, S. P., & Perlman, S. M. (1995) · Virology · doi:10.1006/viro.1995.0021 · Cited by 123 · see citing works
Tumour necrosis factor‐alpha (TNF‐α): The good, the bad and potentially very effective
BARBARA, J. A., Ostade, X. V., & Lopez, A. F. (1996) · Immunology and Cell Biology · doi:10.1038/icb.1996.73 · Cited by 113 · see citing works
Demyelination Determinants Map to the Spike Glycoprotein Gene of Coronavirus Mouse Hepatitis Virus
Sarma, J. D., Fu, L., Tsai, J. C., Weiss, S., & Lavi, E. (2000) · Journal of Virology · doi:10.1128/jvi.74.19.9206-9213.2000 · Cited by 108 · see citing works
Self-citationInterleukin-15 gene expression in human astrocytes and microglia in culture
Lee, Y.-B., Satoh, J., Walker, D. G., & Kim, S. U. (1996) · Neuroreport · doi:10.1097/00001756-199604100-00022 · Cited by 105 · see citing works
Yokota, S., Imagawa, T., Miyamae, T., Ito, S., Nakajima, S., Nezu, A., & Mori, M. (2000) · Pediatrics International · doi:10.1046/j.1442-200x.2000.01204.x · Cited by 104 · see citing works
Lane, T. E., Paoletti, A. D., & Buchmeier, M. J. (1997) · Journal of Virology · doi:10.1128/jvi.71.3.2202-2210.1997 · Cited by 103 · see citing works
Budzilowicz, C., Wilczynski, S. P., & Weiss, S. R. (1985) · Journal of Virology · doi:10.1128/jvi.53.3.834-840.1985 · Cited by 103 · see citing works
Pathogenesis of Multiple Sclerosis—The Immune Diathesis and the Role of Viruses
Allen, I. V., & Brankin, B. (1993) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199303000-00001 · Cited by 102 · see citing works
Lavi, E., Gilden, D. H., Highkin, M. K., & Weiss, S. R. (1984) · Journal of Virology · doi:10.1128/jvi.51.2.563-566.1984 · Cited by 100 · see citing works
Self-citationLimbic encephalitis after inhalation of a murine coronavirus.
Lavi, E., Fishman, P. S., Highkin, M. K., & Weiss, S. R. (1988) · PubMed · Cited by 90 · see citing works
Self-citationGiant cell myocarditis: Most fatal of autoimmune diseases
Rosenstein, E. D., Zucker, M. J., & Kramer, N. (2000) · Seminars in Arthritis and Rheumatism · doi:10.1053/sarh.2000.8367 · Cited by 84 · see citing works
Keck, J., Soe, L. H., Makino, S., Stohlman, S. A., & Lai, M. M. C. (1988) · Journal of Virology · doi:10.1128/jvi.62.6.1989-1998.1988 · Cited by 83 · see citing works
Cytokine dysregulation in HIV-associated neurological disease
Wesselingh, S. L., Glass, J. D., McArthur, J. C., Griffin, J. W., & Griffin, D. E. (1994) · Advances in Neuroimmunology · doi:10.1016/s0960-5428(06)80258-5 · Cited by 82 · see citing works
Phillips, J. J., Chua, M. M., Rall, G. F., & Weiss, S. R. (2002) · Virology · doi:10.1006/viro.2002.1551 · Cited by 82 · see citing works
Komastu, T., Ireland, D. D. C., & Reiss, C. S. (1998) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(98)00017-3 · Cited by 80 · see citing works
Parra, B., Hinton, D. R., Lin, M. T., Cua, D. J., & Stohlman, S. A. (1997) · Virology · doi:10.1006/viro.1997.8613 · Cited by 79 · see citing works
Bystander CD8 T Cell-Mediated Demyelination After Viral Infection of the Central Nervous System
Haring, J. S., Pewe, L. L., & Perlman, S. M. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.3.1550 · Cited by 73 · see citing works
Lavi, E., Suzumura, A., Hirayama, M., Highkin, M. K., Dambach, D. M., Silberberg, D. H., & Weiss, S. R. (1987) · Microbial Pathogenesis · doi:10.1016/0882-4010(87)90066-0 · Cited by 57 · see citing works
Self-citationTsuda, H., & Shirono, K. (1996) · British Journal of Haematology · doi:10.1046/j.1365-2141.1996.d01-1707.x · Cited by 51 · see citing works
Constantinescu, C. S., Hilliard, B. A., Ventura, E. S., Wysocka, M., Showe, L. C., Lavi, E., Fujioka, T., Scott, P., Trinchieri, G., & Rostami, A. M. (2001) · Clinical Immunology · doi:10.1006/clim.2000.4944 · Cited by 51 · see citing works
Self-citationTreatment Strategies for Epstein-Barr Virus-Associated Hemophagocytic Lymphohistiocytosis (EBV-HLH)
Imashuku, S., Tabata, Y., Teramura, T., & Hibi, S. (2000) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428190009053537 · Cited by 49 · see citing works
Suzumura, A., Lavi, E., Bhat, S. Q., Murasko, D. M., Weiss, S. R., & Silberberg, D. H. (1988) · The Journal of Immunology · doi:10.4049/jimmunol.140.6.2068 · Cited by 48 · see citing works
Self-citationThe novel glycoproteins of coronaviruses
Sturman, L. S., & Holmes, K. V. (1985) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(85)90010-6 · Cited by 47 · see citing works
Sarma, J. D., Fu, L., Hingley, S. T., & Lavi, E. (2001) · Experimental and Molecular Pathology · doi:10.1006/exmp.2001.2378 · Cited by 38 · see citing works
Self-citationAránguez, I., Torres, C., & Rubio, N. (1995) · Glia · doi:10.1002/glia.440130305 · Cited by 37 · see citing works
Coronavirus-Induced Demyelination Occurs in the Absence of Inducible Nitric Oxide Synthase
Wu, G. F., Pewe, L. L., & Perlman, S. M. (2000) · Journal of Virology · doi:10.1128/jvi.74.16.7683-7686.2000 · Cited by 36 · see citing works
Inoue, A., Koh, C., Yamazaki, M., Yahikozawa, H., Ichikawa, M., Yagita∥, H., & Kim, B. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.10.5586 · Cited by 35 · see citing works
Lavi, E., Murray, E. M., Makino, S., Stohlman, S. A., Lai, M. M. C., & Weiss, S. R. (1990) · PubMed · Cited by 32 · see citing works
Self-citationLavi, E., Suzumura, A., Murray, E. M., Silberberg, D. H., & Weiss, S. R. (1989) · Journal of Neuroimmunology · doi:10.1016/0165-5728(89)90040-4 · Cited by 28 · see citing works
Self-citationSarma, L. F. J. D. (2001) · Journal of NeuroVirology · doi:10.1080/135502801753170282 · Cited by 25 · see citing works
Nidovirus Infections: Experimental Model Systems of Human Neurologic Diseases
Lavi, E., Schwartz, T., Jin, Y., & Fu, L. (1999) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199912000-00001 · Cited by 22 · see citing works
Self-citationPerrin, P. J., Rumbley, C. A., Beswick, R. L., Lavi, E., & Phillips, S. M. (2000) · Clinical Immunology · doi:10.1006/clim.1999.4825 · Cited by 9 · see citing works
Self-citationFu, L., Sarma, J. D., & Lavi, E. (2001) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-1325-4_98 · Cited by 2 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Nervous system involvement after infection with COVID-19 and other coronaviruses
Wu, Y., Xu, X., Chen, Z., Duan, J., Hashimoto, K., Yang, L., Liu, C., & Yang, C. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.03.031 · Cited by 2,046 · see citing works
Neurologic 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
Ghoshal, A., Das, S., Ghosh, S. K., Mishra, M. K., Sharma, V., Koli, P., Sen, E., & Basu, A. (2007) · Glia · doi:10.1002/glia.20474 · Cited by 387 · see citing works
Girija, A. S. S., Shankar, E. M., & Larsson, M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01206 · Cited by 308 · see citing works
Li, L., Acioglu, C., Heary, R. F., & Elkabes, S. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.10.007 · Cited by 283 · see citing works
Neurological manifestations of long-COVID syndrome: a narrative review
Stefanou, M., Palaiodimou, L., Bakola, E., Smyrnis, N., Papadopoulou, Μ., Paraskevas, G. P., Rizos, E., Boutati, E. I., Grigoriadis, N., Krogias, C., et al. (2022) · Therapeutic Advances in Chronic Disease · doi:10.1177/20406223221076890 · Cited by 260 · see citing works
Does SARS‐Cov‐2 invade the brain? Translational lessons from animal models
Natoli, S., Oliveira, V., Calabresi, P., Maia, L. F., & Pisani, A. (2020) · European Journal of Neurology · doi:10.1111/ene.14277 · Cited by 260 · see citing works
Subjective neurological symptoms frequently occur in patients with SARS-CoV2 infection
Liguori, C., Pierantozzi, M., Spanetta, M., Sarmati, L., Cesta, N., Iannetta, M., Ora, J., Mina, G. G., Puxeddu, E., Balbi, O., et al. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.05.037 · Cited by 212 · see citing works
Biochemical Aspects of Coronavirus Replication and Virus-Host Interaction
Enjuanes, L., Almazán, F., Sola, I., & Zúñiga, S. (2006) · Annual Review of Microbiology · doi:10.1146/annurev.micro.60.080805.142157 · Cited by 223 · see citing works
Song, E., Bartley, C. M., Chow, R. D.-W., Ngo, T. T., Jiang, R., Zamecnik, C. R., Dandekar, R., Loudermilk, R. P., Dai, Y., Liu, F., et al. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100288 · Cited by 212 · see citing works
Neurological Manifestations in COVID-19 Infection: A Systematic Review and Meta-Analysis
Collantes, M. E., Espiritu, A. I., Sy, M. C. C., Anlacan, V. M. M., & Jamora, R. D. G. (2020) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/cjn.2020.146 · Cited by 203 · see citing works
Human coronavirus OC43 infection induces chronic encephalitis leading to disabilities in BALB/C mice
Jacomy, H., Fragoso, G., Almazán, G., Mushynski, W. E., & Talbot, P. J. (2006) · Virology · doi:10.1016/j.virol.2006.01.049 · Cited by 197 · see citing works
Leng, A., Shah, M. M., Ahmad, S. A., Premraj, L., Wildi, K. S., Bassi, G. L., Pardo, C. A., Choi, A., & Cho, S. (2023) · Cells · doi:10.3390/cells12050816 · Cited by 180 · see citing works
COVID-19 and post-infectious myalgic encephalomyelitis/chronic fatigue syndrome: a narrative review
Poenaru, S., Abdallah, S. J., Corrales‐Medina, V., & Cowan, J. (2021) · Therapeutic Advances in Infectious Disease · doi:10.1177/20499361211009385 · Cited by 167 · see citing works
Neuropathobiology of COVID-19: The Role for Glia
Tremblay, M.-E., Madore, C., Bordeleau, M., Tian, L., & Verkhratsky, A. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.592214 · Cited by 159 · see citing works
“In experimental mouse models of infection with coronavirus, MHV-59A resulted in encephalitis with prominent astrogliosis and induction of astroglial synthesis of cytokines; moreover, neurovirulence correlated with the cytokine response (Li et al., 2004).”
BackgroundThe SARS-CoV-2 and mental health: From biological mechanisms to social consequences
Szcześniak, D. M., Gładka, A., Misiak, B., Cyran, A., & Rymaszewska, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110046 · Cited by 152 · see citing works
Jha, N. K., Ojha, S. K., Jha, S. K., Dureja, H., Singh, S. K., Shukla, S. D., Chellappan, D. K., Gupta, G., Bhardwaj, S., Kumar, N., et al. (2021) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01767-6 · Cited by 151 · see citing works
Neurological complications and infection mechanism of SARS-CoV-2
Wan, D., Du, T., Hong, W., Chen, L., Que, H., Lu, S., & Peng, X. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00818-7 · Cited by 132 · see citing works
Does COVID‐19 contribute to development of neurological disease?
Mahalakshmi, A. M., Ray, B., Tuladhar, S., Bhat, A., Paneyala, S., Patteswari, D., Sakharkar, M. K., Hamdan, H., Ojcius, D. M., Bolla, S. R., et al. (2020) · Immunity Inflammation and Disease · doi:10.1002/iid3.387 · Cited by 100 · see citing works
CSF Biomarkers in COVID-19 Associated Encephalopathy and Encephalitis Predict Long-Term Outcome
Guasp, M., Muñoz‐Sánchez, G., Martínez‐Hernández, E., Santana, D., Carbayo, Á., Naranjo, L., Bolós, U., Framil, M., Saiz, A., Balasa, M., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.866153 · Cited by 100 · see citing works
The cytokine storm of COVID-19: a spotlight on prevention and protection
Pearce, L., Davidson, S. M., & Yellon, D. M. (2020) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2020.1783243 · Cited by 99 · 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
Vargas, G., Geraldo, L. H., Salomão, N. G., Paes, M. V., Lima, F. R. S., & Gomes, F. C. A. (2020) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2020.100127 · Cited by 95 · see citing works
The Pathogenesis of Murine Coronavirus Infection of the Central Nervous System
Hosking, M., & Lane, T. E. (2010) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v30.i2.20 · Cited by 93 · see citing works
Murta, V., Villarreal, A., & Ramos, A. J. (2020) · ASN NEURO · doi:10.1177/1759091420954960 · Cited by 89 · see citing works
Abdul-Careem, M. F., Hunter, B. D., Sarson, A. J., Mayameei, A., Zhou, H., & Sharif, S. (2006) · Viral Immunology · doi:10.1089/vim.2006.19.167 · Cited by 88 · see citing works
Cytokine storm induced by SARS-CoV-2 infection: The spectrum of its neurological manifestations
Thepmankorn, P., Bach, J. R., Lasfar, A., Zhao, X., Souayah, S., Chong, Z. Z., & Souayah, N. (2020) · Cytokine · doi:10.1016/j.cyto.2020.155404 · Cited by 86 · see citing works
Neurological Complications of COVID-19: Underlying Mechanisms and Management
Shehata, G. A., Lord, K. C., Grudzinski, M. C., Elsayed, M., Abdelnaby, R., & Elshabrawy, H. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084081 · Cited by 83 · see citing works
COVID-19: dealing with a potential risk factor for chronic neurological disorders
Schirinzi, T., Landi, D., & Liguori, C. (2020) · Journal of Neurology · doi:10.1007/s00415-020-10131-y · Cited by 76 · see citing works
Presentations and mechanisms of CNS disorders related to COVID-19
Bodro, M., Compta, Y., & Sánchez‐Valle, R. (2020) · Neurology Neuroimmunology & Neuroinflammation · doi:10.1212/nxi.0000000000000923 · Cited by 68 · see citing works
Hu, J., Jolkkonen, J., & Zhao, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.012 · Cited by 66 · see citing works
Li, J., Ertel, A., Portocarrero, C. P., Barkhouse, D. A., Dietzschold, B., Hooper, D. C., & Faber, M. (2012) · Journal of Virology · doi:10.1128/jvi.06699-11 · Cited by 65 · see citing works
COVID-19 causes neuronal degeneration and reduces neurogenesis in human hippocampus
Bayat, A., Azimi, H., Moghaddam, M. H., Ebrahimi, V., Fathi, M., Vakili, K. G., Mahmoudiasl, G., Forouzesh, M., Boroujeni, M. E., Nariman, Z., et al. (2022) · APOPTOSIS · doi:10.1007/s10495-022-01754-9 · Cited by 64 · see citing works
SARS-CoV-2, an Underestimated Pathogen of the Nervous System
Jakhmola, S., Indari, O., Chatterjee, S., & Jha, H. C. (2020) · SN Comprehensive Clinical Medicine · doi:10.1007/s42399-020-00522-7 · Cited by 64 · see citing works
Awogbindin, I. O., Ben‐Azu, B., Olusola, B. A., Akinluyi, E. T., Adeniyi, P. A., Paolo, T. D., & Tremblay, M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.670298 · Cited by 60 · see citing works
Cascella, M., Gaudio, A. D., Vittori, A., Bimonte, S., Prete, P. D., Forte, C. A., Cuomo, A., & Blasio, E. D. (2021) · Journal of Pain Research · doi:10.2147/jpr.s313978 · Cited by 62 · see citing works
A Mechanism of Virus-Induced Demyelination
Sarma, J. D. (2010) · Interdisciplinary Perspectives on Infectious Diseases · doi:10.1155/2010/109239 · Cited by 14 · see citing works
Lavi, E., & Cong, L. (2020) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2020.104474 · Cited by 59 · see citing works
Self-citationSevere acute respiratory syndrome coronavirus 2 infection reaches the human nervous system: How?
Uversky, V. N., Elrashdy, F., Aljaddawi, A. A., Ali, S. M., Khan, R. H., & Redwan, E. M. M. M. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24752 · Cited by 57 · see citing works
Impact of COVID-19 on Alzheimer’s Disease Risk: Viewpoint for Research Action
Abate, G., Memo, M., & Uberti, D. (2020) · Healthcare · doi:10.3390/healthcare8030286 · Cited by 56 · see citing works
Specific EEG Encephalopathy Pattern in SARS-CoV-2 Patients
Pastor, J., Vega-Zelaya, L., & Abad, E. M. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9051545 · Cited by 55 · see citing works
Meessen-Pinard, M., Coupanec, A. L., Desforges, M., & Talbot, P. J. (2016) · Journal of Virology · doi:10.1128/jvi.01513-16 · Cited by 50 · see citing works
Chen, X., Quan, R., Guo, X.-K., Gao, L., Shi, J. N., & Feng, W.-H. (2014) · Veterinary Microbiology · doi:10.1016/j.vetmic.2014.01.031 · Cited by 50 · see citing works
The Social Brain and Emotional Contagion: COVID-19 Effects
Valenzano, A. A., Scarinci, A., Monda, V., Sessa, F., Messina, A., Monda, M., Precenzano, F., Mollica, M. P., Carotenuto, M., Messina, G., et al. (2020) · Medicina · doi:10.3390/medicina56120640 · Cited by 49 · see citing works
Post-Acute COVID-19 Neurological Syndrome: A New Medical Challenge
Nuzzo, D., Vasto, S., Scalisi, L., Cottone, S., Cambula, G., Rizzo, M., Giacomazza, D., & Picone, P. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10091947 · Cited by 49 · see citing works
Marcondes, M. C. G., Burdo, T. H., Sopper, S., Huitrón‐Reséndiz, S., Lanigan, C. M. S., Watry, D. D., Flynn, C. T., Zandonatti, M. A., & Fox, H. S. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.9.5812 · Cited by 49 · see citing works
Viral Induction of Central Nervous System Innate Immune Responses
Rempel, J. D., Quina, L. A., Blakely-Gonzales, P., Buchmeier, M. J., & Gruol, D. L. (2005) · Journal of Virology · doi:10.1128/jvi.79.7.4369-4381.2005 · Cited by 48 · see citing works
Neurobiology of coronaviruses: Potential relevance for COVID-19
Cataldi, M., Pignataro, G., & Taglialatela, M. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105007 · Cited by 47 · see citing works
The Impact of the COVID-19 Pandemic on Dementia Risk: Potential Pathways to Cognitive Decline
Pyne, J. D., & Brickman, A. M. (2021) · Neurodegenerative Diseases · doi:10.1159/000518581 · Cited by 48 · see citing works
Neuroinvasion of SARS‐CoV‐2 may play a role in the breakdown of the respiratory center of the brain
Dey, J., Alam, M. T., Chandra, S., Gupta, J., Ray, U., Srivastava, A. K., & Tripathi, P. P. (2021) · Journal of Medical Virology · doi:10.1002/jmv.26521 · Cited by 43 · see citing works
Haidar, M. A., Jourdi, H., Hassan, Z. H., Ashekyan, O., Fardoun, M., Wehbe, Z., Maaliki, D. S., Wehbe, M., Mondello, S., Abdelhady, S., et al. (2021) · The Neuroscientist · doi:10.1177/1073858420984106 · Cited by 43 · see citing works
Caì, Y., Liu, Y., & Zhang, X. (2006) · Virology · doi:10.1016/j.virol.2006.07.012 · Cited by 40 · see citing works
Archie, S. R., & Cucullo, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113916 · Cited by 37 · 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
Coronavirus disease 2019 and neurodegenerative disease: what will the future bring?
McAlpine, L. S., Fesharaki‐Zadeh, A., & Spudich, S. (2020) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000688 · Cited by 34 · see citing works
COVID-19-Induced Neurovascular Injury: a Case Series with Emphasis on Pathophysiological Mechanisms
Amezcua, J. M. G., Jain, R., Kleinman, G., Muh, C. R., Guzzetta, M., Folkerth, R. D., Snuderl, M., Placantonakis, D. G., Galetta, S. L., Hochman, S. E., et al. (2020) · SN Comprehensive Clinical Medicine · doi:10.1007/s42399-020-00598-1 · Cited by 33 · see citing works
Complications and Pathophysiology of COVID-19 in the Nervous System
Yu, H., Sun, T., & Feng, J. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.573421 · Cited by 33 · see citing works
What can neuroimmunology teach us about the symptoms of long-COVID?
Mondelli, V., & Pariante, C. M. (2021) · Oxford Open Immunology · doi:10.1093/oxfimm/iqab004 · Cited by 32 · see citing works
Emerging potential mechanisms and predispositions to the neurological manifestations of COVID-19
Jesuthasan, A., Massey, F., Manji, H., Zandi, M. S., & Wiethoff, S. (2021) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2021.117608 · Cited by 32 · see citing works
Cellular and Molecular Effects of SARS-CoV-2 Linking Lung Infection to the Brain
Francistiová, L., Klepe, A., Curley, G., Gulya, K., Dinnyés, A., & Filkor, K. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.730088 · Cited by 32 · see citing works
Chen, X., Zhang, G., Li, Y., Xing, F., Wan, F., Zhang, L., Wang, J., & Zhang, X. (2008) · Journal of Molecular Neuroscience · doi:10.1007/s12031-008-9133-z · Cited by 31 · see citing works
Self-citationYu, D., Zhu, H., Liu, Y., Cao, J., & Zhang, X. (2009) · Journal of Virology · doi:10.1128/jvi.01103-09 · Cited by 31 · see citing works
Zuo, J., Stohlman, S. A., Hoskin, J. B., Hinton, D. R., Atkinson, R., & Bergmann, C. C. (2006) · Virology · doi:10.1016/j.virol.2006.01.027 · Cited by 31 · see citing works
COVID-19 and neurocognitive disorders
Mukaetova-Ladinska, E. B., Kronenberg, G., & Raha‐Chowdhury, R. (2020) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000687 · Cited by 28 · see citing works
The case of encephalitis in a COVID-19 pediatric patient
Urso, L., Distefano, M. G., Cambula, G., Colomba, A., Nuzzo, D., Picone, P., Giacomazza, D., & Sicurella, L. (2021) · Neurological Sciences · doi:10.1007/s10072-021-05670-9 · Cited by 28 · see citing works
Versteeg, G. A., Slobodskaya, O. R., & Spaan, W. J. M. (2006) · Journal of General Virology · doi:10.1099/vir.0.81756-0 · Cited by 27 · see citing works
Neuro-COVID-19: an insidious virus in action
Bratosiewicz‐Wąsik, J. (2021) · Neurologia i Neurochirurgia Polska · doi:10.5603/pjnns.a2021.0072 · Cited by 26 · see citing works
Filho, A. J. M. C., Gonçalves, F., Mottin, M., Andrade, C. H., Fonseca, S. N. S., & Macêdo, D. S. (2021) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-021-09986-3 · Cited by 24 · see citing works
Effects and Causes of Detraining in Athletes Due to COVID-19: A Review
Córdova, A., Caballero-García, A., Roche, E., Pérez-Valdecantos, D., & Noriega, D. C. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19095400 · Cited by 26 · see citing works
Frailty after COVID ‐19: The wave after?
König, M., Gollasch, M., & Komleva, Y. (2023) · Aging Medicine · doi:10.1002/agm2.12258 · Cited by 23 · see citing works
Rodriguez, M., Soler, Y., Pokharel, M. D., Reynolds, J. L., & El‐Hage, N. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.583459 · Cited by 22 · see citing works
ELBini-Dhouib, I. (2020) · Drug Discoveries & Therapeutics · doi:10.5582/ddt.2020.03106 · Cited by 19 · see citing works
Neuroinvasive potential of a primary respiratory pathogen SARS- CoV2: Summarizing the evidences
Lahiri, D., Mondal, R., Deb, S., Bandyopadhyay, D., Shome, G., Sarkar, S., & Biswas, S. C. (2020) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2020.06.062 · Cited by 19 · see citing works
Crosstalk Between Lung and Extrapulmonary Organs in Infection and Inflammation
Wang, Z., Pu, Q., Huang, C., & Wu, M. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-63046-1_18 · Cited by 18 · see citing works
COVID-19 and central nervous system interplay: A big picture beyond clinical manifestation
Chaudhury, S. S., Sinha, K., Majumder, R., Biswas, A., & Mukhopadhyay, C. D. (2021) · Journal of Biosciences · doi:10.1007/s12038-021-00165-3 · Cited by 19 · see citing works
Valizadeh, P., Momtazmanesh, S., Plazzi, G., & Rezaei, N. (2023) · Sleep Medicine · doi:10.1016/j.sleep.2023.12.005 · Cited by 18 · see citing works
Putative mechanism of neurological damage in COVID-19 infection
Bandala, C., Cortes-Altamirano, J. L., Reyes-Long, S., Lara‐Padilla, E., Ilizaliturri‐Flores, I., & Alfaro-Rodríguez, A. (2021) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2021-008 · Cited by 17 · see citing works
COVID-19 and Central Nervous System: Entry Routes And Probable Damages
Ahmadirad, N., & Ghasemi, Z. (2020) · Basic and Clinical Neuroscience Journal · doi:10.32598/bcn.11.covid19.2360.1 · Cited by 16 · see citing works
Gruslin, E., Moisan, S., St‐Pierre, Y., Desforges, M., & Talbot, P. J. (2005) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.01.007 · Cited by 15 · see citing works
Wu, J., & Tang, Y. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.566680 · Cited by 14 · see citing works
Lima, M., Aloizou, A., Siokas, V., Bakirtzis, C., Liampas, I., Tsouris, Z., Bogdanos, D. P., Balogiannis, S., & Dardiotis, E. (2022) · Reviews in the Neurosciences · doi:10.1515/revneuro-2021-0148 · Cited by 33 · see citing works
Rahmani, B., Ghashghaei, E., Zendehdel, M., Baghbanzadeh, A., & Khodadadi, M. (2022) · Physiology International · doi:10.1556/2060.2022.00019 · Cited by 13 · see citing works
Current Perspective of COVID-19 on Neurology: A Mechanistic Insight
Mathew, B., Kumar, R., Harilal, S., Sabitha, M., Pappachen, L. K., & Roshni, P. R. (2021) · Combinatorial Chemistry & High Throughput Screening · doi:10.2174/1386207324666210805121828 · Cited by 13 · see citing works
The neuropathological impact of COVID-19: a review
Fouad, G. I. (2021) · Bulletin of the National Research Centre/Bulletin of the National Research Center · doi:10.1186/s42269-020-00478-7 · Cited by 11 · see citing works
Mouse hepatitis virus infection of the CNS: a model for defense, disease, and repair
Chris, S. S. (2008) · Frontiers in bioscience · doi:10.2741/3012 · Cited by 11 · see citing works
Scott, E. P., Branigan, P. J., Vecchio, A. M. D., & Weiss, S. R. (2008) · Journal of NeuroVirology · doi:10.1080/13550280701750635 · Cited by 11 · see citing works
Astrocyte expression of a dominant‐negative interferon‐γ receptor
Hindinger, C., González, J., Bergmann, C., Fuss, B., Hinton, D., Atkinson, R., Macklin, W., & Stohlman, S. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20616 · Cited by 12 · see citing works
Ahmadi, S., & Khaledi, S. (2023) · Analytical Cellular Pathology · doi:10.1155/2023/8883492 · Cited by 11 · see citing works
Wang, L., Ren, Z., Ma, L., Han, Y., Wei, W., Jiang, E., & Ji, X.-Y. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2020.592888 · Cited by 10 · see citing works
Pathophysiology of COVID-19-Associated Neurotoxicity
Cascella, M., & Blasio, E. D. (2021) · Springer eBooks · doi:10.1007/978-3-030-86705-8_1 · Cited by 8 · see citing works
Valdes, E., Agarwal, S., Carroll, E. E., Kvernland, A., Bondi, S., Snyder, T. E., Kwon, P. M., Frontera, J. A., Gurin, L. J., Czeisler, B. M., et al. (2020) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2020.117087 · Cited by 8 · see citing works
Rajayer, S. R., & Smith, S. M. (2023) · Intensive Care Medicine Experimental · doi:10.1186/s40635-023-00557-9 · Cited by 7 · see citing works
The Impact of COVID-19 on People Living with HIV-1 and HIV-1-Associated Neurological Complications
Dutta, D., Liu, J., & Xiong, H. (2023) · Viruses · doi:10.3390/v15051117 · Cited by 7 · see citing works
Niemczak, C. E., Ford, J., Roth, R. M., Leigh, S. M., Parsonnet, J., Martin, C. Y., Soule, S. O., Haron, T. M., Buckey, J. C., & Wylie, G. R. (2024) · Brain and Cognition · doi:10.1016/j.bandc.2024.106254 · Cited by 7 · see citing works
Chong, Z.-Z., & Souayah, N. (2021) · Current Medicinal Chemistry · doi:10.2174/0929867328666210506161543 · Cited by 7 · see citing works
COVID-19 and its impact on the brain and Mind- A conceptual model and supporting evidence
Saeed, S. A., Pastis, I., & Santos, M. G. (2022) · Psychiatric Quarterly · doi:10.1007/s11126-022-09980-9 · Cited by 7 · see citing works
COVID-19 Worsens Chronic Lumbosacral Radicular Pain—Case Series Report
Illéš, R., Chochol, J., Džubera, A., Chocholová, A., & Zemková, E. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19116410 · Cited by 6 · see citing works
Outcomes of RIP Kinase Signaling During Neuroinvasive Viral Infection
Daniels, B. P., & Oberst, A. (2020) · Current topics in microbiology and immunology · doi:10.1007/82_2020_204 · Cited by 5 · see citing works
Yu, D., & Zhang, X. (2006) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-33012-9_73 · Cited by 6 · see citing works
DJ-1-Nrf2 axis is activated upon murine β-coronavirus infection in the CNS
Kundu, S., Saadi, F., Sengupta, S., Antony, G. R., Raveendran, V. A., Kumar, R., Kamble, M., Sarkar, L., Burrows, A. C., Pal, D., et al. (2021) · Brain Disorders · doi:10.1016/j.dscb.2021.100021 · Cited by 6 · see citing works
- Authors
- Li, Y., Fu, L., Gonzales, D. M., & Lavi, E.
- Affiliations
- University of Pennsylvania (US)
- NewYork–Presbyterian Hospital (US)
- Corresponding author
- Lavi, Ehud
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2004-04
- Volume
- 78
- Issue
- 7
- Pages
- 3398-3406
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC371061
- OpenAlex
- W2126255553
- Cited by
- 158
- References
- 61
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 9 · 2023: 13 · 2022: 15 · 2021: 38 · 2020: 49 · 2018: 1 · 2016: 1 · 2014: 3 · 2012: 1
- FWCI
- 3.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Multiple Sclerosis Society
- Multiple Sclerosis Society
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS-30606, P01NS030606)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Keywords
- mouse hepatitis virus, astrocytes, microglia, inflammatory cytokines, IL-12, TNF-α, interleukin-6, IL-15, IL-1β, central nervous system infection, neuroinflammation
- MeSH terms
- Animals, Astrocytes, Cells, Cultured, Gene Expression Regulation, Mice, Inbred C57BL, RNA, Messenger, Virulence, Virus Replication, Cytokines, Microglia, Coronavirus, Inflammation Mediators, Oligonucleotide Array Sequence Analysis, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
