Neurological sequelae induced by alphavirus infection of the CNS are attenuated by treatment with the glutamine antagonist 6-diazo-5-oxo-l-norleucine
Open accessAbstract
Recovery from encephalomyelitis induced by infection with mosquito-borne alphaviruses is associated with a high risk of lifelong debilitating neurological deficits. Infection of mice with the prototypic alphavirus, Sindbis virus, provides an animal model with which to study disease mechanisms and examine potential therapeutics. Infectious virus is cleared from the brain within a week after infection, but viral RNA is cleared slowly and persists for the life of the animal. However, no studies have examined the effect of infection on neurocognitive function over time. In the present study, we examined neurocognitive function at different phases of infection in 5-week-old C57BL/6 mice intranasally inoculated with Sindbis virus. At the peak of active virus infection, mice demonstrated hyperactivity, decreased anxiety, and marked hippocampal-dependent memory deficits, the latter of which persisted beyond clearance of infectious virus and resolution of clinical signs of disease. Previous studies indicate that neuronal damage during alphavirus encephalomyelitis is primarily due to inflammatory cell infiltration and glutamate excitotoxicity rather than directly by virus infection. Therefore, mice were treated with 6-diazo-5-oxo-l-norleucine (DON), a glutamine antagonist that can suppress both the immune response and excitotoxicity. Treatment with DON decreased inflammatory cell infiltration and cell death in the hippocampus and partially prevented development of clinical signs and neurocognitive impairment despite the presence of infectious virus and high viral RNA levels. This study presents the first report of neurocognitive sequelae in mice with alphavirus encephalomyelitis and provides a model system for further elucidation of the pathogenesis of virus infection and assessment of potential therapies.
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Research on mice inoculated with encephalitic viruses has demonstrated significant hippocampal impairment and memory deficits, as evidenced by fear conditioning tests and active avoidance experiments.
“Furthermore, research on mice inoculated with encephalitic viruses has demonstrated significant hippocampal impairment and memory deficits, as evidenced by fear conditioning tests (Potter et al., 2015) and active avoidance experiments.”
From Arbovirus infection increases the risk for the development of neurodegenerative disease pathology in the murine model (2024) · cites this paper as Potter et al., 2015
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Cites
Glutamate neurotoxicity and diseases of the nervous system
Choi, D. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90162-6 · Cited by 8,152 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.274 · Cited by 3,262 · see citing works
The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation
Wang, R., Dillon, C. P., Shi, L. Z., Milasta, S., Carter, R., Finkelstein, D., McCormick, L. L., Fitzgerald, P., Chi, H., Munger, J., et al. (2011) · Immunity · doi:10.1016/j.immuni.2011.09.021 · Cited by 2,140 · cited 5× · see citing works
“…administration of a glutamine antagonist, DON, which affects two different mechanisms known to contribute to the pathology seen during SINV infection: inflammatory damage induced by the immune response and glutamate excitotoxicity (Newsholme et al. 1985; Greene et al. 2008; Wang et al. 2011).”
BackgroundInfluentialPresent and future arboviral threats
Weaver, S. C., & Reisen, W. K. (2009) · Antiviral Research · doi:10.1016/j.antiviral.2009.10.008 · Cited by 1,567 · see citing works
The contextual brain: implications for fear conditioning, extinction and psychopathology
Maren, S., Phan, K. L., & Liberzon, I. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3492 · Cited by 1,547 · see citing works
The Global Emergence/Resurgence of Arboviral Diseases As Public Health Problems
Gubler, D. J. (2002) · Archives of Medical Research · doi:10.1016/s0188-4409(02)00378-8 · Cited by 1,140 · see citing works
(2000) · Cited by 919 · see citing works
Consequences of the Expanding Global Distribution of Aedes albopictus for Dengue Virus Transmission
Lambrechts, L., Scott, T. W., & Gubler, D. J. (2010) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000646 · Cited by 780 · see citing works
Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells
Nadler, J. V., Perry, B. W., & Cotman, C. W. (1978) · Nature · doi:10.1038/271676a0 · Cited by 745 · see citing works
Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review
Kim, J. J., & Jung, M. W. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.005 · Cited by 636 · see citing works
Phillips, R. G., & LeDoux, J. E. (1994) · Learning & Memory · doi:10.1101/lm.1.1.34 · Cited by 528 · see citing works
Ecology and Geographical Expansion of Japanese Encephalitis Virus
van den Hurk, A. F., Ritchie, S. A., & Mackenzie, J. S. (2008) · Annual Review of Entomology · doi:10.1146/annurev.ento.54.110807.090510 · Cited by 508 · see citing works
What's Wrong With My Mouse?: Behavioral Phenotyping of Transgenic and Knockout Mice
Crawley, J. N. (2007) · doi:10.1002/0470119055 · Cited by 474 · cited 2× · see citing works
“In addition, the hippocampus plays a very important role in cognition, and factors affecting learning and memory processes can be probed using tasks such as fear conditioning (Crawley 2007; Maren et al. 2013).”
BackgroundGLUTAMINE METABOLISM IN LYMPHOCYTES: ITS BIOCHEMICAL, PHYSIOLOGICAL AND CLINICAL IMPORTANCE
Newsholme, E. A., Crabtree, B., & Ardawi, M. S. M. (1985) · Quarterly Journal of Experimental Physiology · doi:10.1113/expphysiol.1985.sp002935 · Cited by 465 · see citing works
Human immunodeficiency virus‐associated neurocognitive disorders: Mind the gap
McArthur, J. C., Steiner, J. P., Sacktor, N. C., & Nath, A. (2010) · Annals of Neurology · doi:10.1002/ana.22053 · Cited by 445 · see citing works
Logue, S. F., Paylor, R., & Wehner, J. M. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.1.104 · Cited by 385 · see citing works
Logue, S. F., Paylor, R. E., & Wehner, J. M. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.1.104 · Cited by 379 · see citing works
Antibody-Mediated Clearance of Alphavirus Infection From Neurons
Levine, B., Hardwick, J. M., Trapp, B. D., Crawford, T. O., Bollinger, R. C., & Griffin, D. E. (1991) · Science · doi:10.1126/science.1658936 · Cited by 361 · see citing works
Self-citationContext Fear Learning in the Absence of the Hippocampus
Wiltgen, B. J., Sanders, M. J., Anagnostaras, S., Sage, J. R., & Fanselow, M. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2685-05.2006 · Cited by 349 · see citing works
The place of the hippocampus in fear conditioning
Sanders, M. J., Wiltgen, B. J., & Fanselow, M. S. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01283-4 · Cited by 316 · see citing works
Marlatt, M. W., Potter, M. C., Lucassen, P. J., & van Praag, H. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22009 · Cited by 314 · see citing works
Self-citationAcute dendrotoxic changes in the hippocampus of kainate treated rats
Olney, J. W., Fuller, T., & De Gubareff, T. (1979) · Brain Research · doi:10.1016/0006-8993(79)90872-2 · Cited by 300 · see citing works
Souba, W. W. (1993) · Annals of Surgery · doi:10.1097/00000658-199312000-00004 · Cited by 294 · see citing works
Re-emergence of epidemic Venezuelan equine encephalomyelitis in South America
Weaver, S. C., Salas, R., Rico-Hesse, R., Ludwig, G. V., Oberste, M. S., Boshell, J., & Tesh, R. B. (1996) · The Lancet · doi:10.1016/s0140-6736(96)02275-1 · Cited by 285 · see citing works
Molecular basis of Sindbis virus neurovirulence in mice
Lustig, S., Jackson, A. C., Hahn, C. S., Griffin, D. E., Strauss, E. G., & Strauss, J. H. (1988) · Journal of Virology · doi:10.1128/jvi.62.7.2329-2336.1988 · Cited by 253 · see citing works
Self-citationInterferon-γ-Mediated Site-Specific Clearance of Alphavirus from CNS Neurons
Binder, G. K., & Griffin, D. E. (2001) · Science · doi:10.1126/science.1059742 · Cited by 252 · see citing works
Self-citationJurgens, H. A., Amancherla, K., & Johnson, R. W. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.6389-11.2012 · Cited by 243 · see citing works
Etiologic classification of attention-deficit/hyperactivity disorder.
Millichap, J. G. (2008) · PEDIATRICS · doi:10.1542/peds.2007-1332 · Cited by 234 · see citing works
Contextual conditioning and auditory cue conditioning dissociate during development.
Rudy, J. W. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.5.887 · Cited by 220 · see citing works
Muscimol Inactivation of the Dorsal Hippocampus Impairs Contextual Retrieval of Fear Memory
Holt, W., & Maren, S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-09054.1999 · Cited by 213 · see citing works
Toll-like receptor 3 inhibits memory retention and constrains adult hippocampal neurogenesis
Okun, E., Griffioen, K. J. S., Barak, B., Roberts, N. J., Castro, K., Pita, M. A., Cheng, A., Mughal, M. R., Wan, R., Ashery, U., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005807107 · Cited by 207 · see citing works
Distributed circuits underlying anxiety
Adhikari, A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00112 · Cited by 204 · see citing works
A Behavioral and Cognitive Profile of Clinically Stable HIV-Infected Children
Nozyce, M. L., Lee, S. S., WIZNIA, A. A., Nachman, S., MOFENSON, L. M., Smith, M. E., Yogev, R., McIntosh, K., Stanley, K., & Pelton, S. I. (2006) · PEDIATRICS · doi:10.1542/peds.2005-0451 · Cited by 182 · see citing works
Fitting, S., Ignatowska-Jankowska, B. M., Bull, C., Skoff, R. P., Lichtman, A. H., Wise, L. E., Fox, M. A., Su, J., Medina, A. E., Krahe, T. E., et al. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.026 · Cited by 162 · see citing works
Medical Aspects of Biological Warfare
Lillibridge, S. R. (2008) · JAMA · doi:10.1001/jama.300.6.735 · Cited by 156 · see citing works
Melnikova, T., Savonenko, A. V., Wang, Q., Liang, X., Hand, T. A., Wu, L., Kaufmann, W. E., Vehmas, A. K., & Andreasson, K. I. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.001 · Cited by 134 · see citing works
Persistence of viral RNA in mouse brains after recovery from acute alphavirus encephalitis
Levine, B., & Griffin, D. E. (1992) · Journal of Virology · doi:10.1128/jvi.66.11.6429-6435.1992 · Cited by 126 · see citing works
Self-citationColombo, S. L., Palacios‐Callender, M., Frakich, N., de León, J., Schmitt, C. A., Boorn, L., Davis, N., & Moncada, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012362107 · Cited by 126 · see citing works
HIV-associated neurocognitive disorders
Sanmartí, M., Ibáñez, L., Huertas, S., Badenes, D., Dalmau, D., SLEVIN, M. A., Krupiński, J., Popa‐Wagner, A., & Jaén, Á. (2014) · Journal of Molecular Psychiatry · doi:10.1186/2049-9256-2-2 · Cited by 106 · see citing works
Glutamine targeting inhibits systemic metastasis in the VM‐M3 murine tumor model
Shelton, L. M., Huysentruyt, L. C., & Seyfried, T. N. (2010) · International Journal of Cancer · doi:10.1002/ijc.25431 · Cited by 102 · see citing works
Targeting the Glutamatergic System for the Treatment of HIV-Associated Neurocognitive Disorders
Potter, M. C., Figuera-Losada, M., Rojas, C. J., & Slusher, B. S. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9442-z · Cited by 93 · see citing works
Self-citationJin, S.-J., Takeuchi, H., Yawata, I., Harada, Y., Sonobe, Y., Doi, Y., Liang, J.-F., Hua, L., Yasuoka, S., Zhou, Y., et al. (2009) · Tohoku journal of experimental medicine · doi:10.1620/tjem.217.87 · Cited by 92 · see citing works
Jackson, A. C., Moench, T. R., Griffin, D. E., & Rt, J. (1987) · PubMed · Cited by 91 · see citing works
Self-citationThe Economic Burden Imposed by a Residual Case of Eastern Encephalitis
Villari, P., Spielman, A., Komar, N., McDowell, M., & Timperi, R. (1995) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1995.52.8 · Cited by 89 · see citing works
Emergence and re-emergence of viral diseases of the central nervous system
Griffin, D. E. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.12.003 · Cited by 83 · see citing works
Self-citationMetcalf, T. U., & Griffin, D. E. (2011) · Journal of Virology · doi:10.1128/jvi.05379-11 · Cited by 77 · see citing works
Self-citationGlutamate receptor antagonists protect from virus‐induced neural degeneration
Nargi‐Aizenman, J. L., Havert, M. B., Zhang, M., Irani, D. N., Rothstein, J. D., & Griffin, D. E. (2004) · Annals of Neurology · doi:10.1002/ana.20033 · Cited by 76 · see citing works
Self-citationEarhart, R. H., Amato, D. J., Chang, A. Y.-C., Borden, E. C., Shiraki, M., Dowd, M. E., Comis, R. L., Davis, T. E., & Smith, T. J. (1990) · Investigational New Drugs · doi:10.1007/bf00216936 · Cited by 71 · see citing works
:Medical Aspects of Biological Warfare
Grönvall, G. K. (2009) · Clinical Infectious Diseases · doi:10.1086/595853 · Cited by 71 · see citing works
Exercise is not beneficial and may accelerate symptom onset in a mouse model of Huntington’s disease
Potter, M. C., Yuan, C., Ottenritter, C., Mughal, M. R., & van Praag, H. (2010) · PLoS Currents · doi:10.1371/currents.rrn1201 · Cited by 68 · see citing works
Self-citationEastern Equine Encephalitis in Children, Massachusetts and New Hampshire,USA, 1970–2010
Silverman, M. A., Misasi, J., Smole, S., Feldman, H. A., Cohen, A. B., Santagata, S., McManus, M. L., & Ahmed, A. A. (2013) · Emerging infectious diseases · doi:10.3201/eid1902.120039 · Cited by 67 · see citing works
Umpierre, A. D., Remigio, G. J., Dahle, E. J., Bradford, K., Alex, A. B., Smith, M. D., West, P. J., White, H. S., & Wilcox, K. S. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.12.015 · Cited by 66 · see citing works
Neurologic, intellectual, and psychologic sequelae following western encephalitis
Earnest, M. P., Goolishian, H. A., Calverley, J. R., Hayes, R. O., & Hill, H. R. (1971) · Neurology · doi:10.1212/wnl.21.9.969 · Cited by 66 · see citing works
Havert, M. B., Schofield, B., Griffin, D. E., & Irani, D. N. (2000) · Journal of Virology · doi:10.1128/jvi.74.11.5352-5356.2000 · Cited by 63 · see citing works
Self-citationAmaral, D. C. G., Rachid, M. A., Vilela, M. C., Campos, R. D. L., Ferreira, G. P., Rodrigues, D. H., Lacerda‐Queiroz, N., de Miranda, A. S., Costa, V. V., Campos, M. A., et al. (2011) · Journal of Neuroinflammation · doi:10.1186/1742-2094-8-23 · Cited by 62 · see citing works
Gould, T. J., McCarthy, M. M., & Keith, R. A. (2002) · Behavioural Pharmacology · doi:10.1097/00008877-200207000-00005 · Cited by 60 · see citing works
Kimura, T., & Griffin, D. E. (2003) · Virology · doi:10.1016/s0042-6822(03)00110-7 · Cited by 51 · see citing works
Self-citationGreene, I. P., Lee, E.-Y., Prow, N. A., Ngwang, B., & Griffin, D. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712390105 · Cited by 50 · see citing works
Self-citationRowell, J. F., & Griffin, D. E. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.3.1624 · Cited by 50 · see citing works
Self-citationExtrahippocampal Involvement in Human Herpesvirus 6 Encephalitis Depicted at MR Imaging
Provenzale, J. M., VanLandingham, K., Lewis, D. V., Mukundan, S., & WHITE, L. E. (2008) · Radiology · doi:10.1148/radiol.2492071917 · Cited by 47 · see citing works
Goeldner, C., Reiss, D., Wichmann, J., Kieffer, B. L., & Ouagazzal, A. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.12.001 · Cited by 46 · see citing works
Western Equine and St. Louis Encephalitis
Finley, K. H., LONGSHORE, W. A., Palmer, R. J., Cook, R. E., & Riggs, N. (1955) · Neurology · doi:10.1212/wnl.5.4.233 · Cited by 43 · see citing works
Phase I study of 6-diazo-5-oxo-L-norleucine (DON).
Sklaroff, R. B., Casper, E. S., Magill, G. B., & Cw, Y. (1980) · PubMed · Cited by 29 · see citing works
Phase I and pharmacokinetic studies of DON.
Kovach, J. S., Eagan, R. T., Powis, G., Rubin, J., Creagan, E. T., & Moertel, C. G. (1981) · PubMed · Cited by 26 · see citing works
Phase I trial of 6-diazo-5-oxo-L-norleucine (DON) administered by 5-day courses.
Earhart, R. H., Koeller, J. M., & Davis, H. L. (1982) · PubMed · Cited by 23 · see citing works
Western equine encephalitis in infants; a report on three cases with sequelae.
Bruyn, H. B., & Lennette, E. H. (1953) · PubMed · Cited by 14 · see citing works
Flagged first, then by citations
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- Griffin DE Knipe DM Howley PM 2013 Alphaviruses Fields Virology 6 Lippincott Williams & Wilkins Philadelphia 652 686
Cited by
Sorted by citations
Rais, R., Jančařík, A., Tenora, L., Nedelcovych, M., Alt, J., Englert, J., Rojas, C., Le, A., Elgogary, A., Tan, J., et al. (2016) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b01069 · Cited by 138 · see citing works
Self-citationClark, I. A., & Vissel, B. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0708-2 · Cited by 123 · see citing works
Microglial glutaminase 1 deficiency mitigates neuroinflammation associated depression
Ji, C., Tang, Y., Zhang, Y., Li, C., Liang, H., Ding, L., Xia, X., Xiong, L., Qi, X., & Zheng, J. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.10.009 · Cited by 79 · see citing works
Nedelcovych, M. T., Tenora, L., Kim, B.-H., Kelschenbach, J., Chao, W., Hadas, E., Jančařík, A., Prchalová, E., Zimmermann, S. C., Dash, R. P., et al. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.7b00966 · Cited by 66 · see citing works
Self-citationImmunopathogenesis of alphaviruses
Baxter, V. K., & Heise, M. (2020) · Advances in Virus Research · doi:10.1016/bs.aivir.2020.06.002 · Cited by 45 · see citing works
Self-citationHost cell glutamine metabolism as a potential antiviral target
Hirabara, S. M., Gorjão, R., Levada‐Pires, A. C., Masi, L. N., Hatanaka, E., Cury‐Boaventura, M. F., da Silva, E. B., dos Santos-Oliveira, L. C., Diniz, V. L. S., Serdan, T. D. A., et al. (2021) · Clinical Science · doi:10.1042/cs20201042 · Cited by 55 · see citing works
Zhu, X., Nedelcovych, M. T., Thomas, A. G., Hasegawa, Y., Moreno-Megui, A., Coomer, W., Vohra, V., Saito, A., Perez, G., Wu, Y., et al. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0177-7 · Cited by 53 · see citing works
Self-citationImplications of Innate Immunity in Post-Acute Sequelae of Non-Persistent Viral Infections
Hirschenberger, M., Hunszinger, V., & Sparrer, K. M. J. (2021) · Cells · doi:10.3390/cells10082134 · Cited by 49 · see citing works
Manivannan, S., Baxter, V. K., Schultz, K. L. W., Slusher, B. S., & Griffin, D. E. (2016) · Journal of Virology · doi:10.1128/jvi.01045-16 · Cited by 36 · see citing works
Self-citationMRI demonstrates glutamine antagonist-mediated reversal of cerebral malaria pathology in mice
Riggle, B. A., Sinharay, S., Schreiber-Stainthorp, W., Munasinghe, J., Maric, D., Prchalová, E., Slusher, B. S., Powell, J. D., Miller, L. H., Pierce, S. K., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1812909115 · Cited by 34 · see citing works
Self-citationLemberg, K. M., Zhao, L., Wu, Y., Veeravalli, V., Alt, J., Aguilar, J. M. H., Dash, R. P., Lam, J., Tenora, L., Rodriguez, C., et al. (2019) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-19-0319 · Cited by 30 · see citing works
Self-citationBaxter, V. K., & Griffin, D. E. (2016) · Journal of General Virology · doi:10.1099/jgv.0.000613 · Cited by 29 · see citing works
Self-citationNilaratanakul, V., Chen, J., Tran, O., Baxter, V. K., Troisi, E. M., Yeh, J. X., & Griffin, D. E. (2018) · Journal of Virology · doi:10.1128/jvi.02081-17 · Cited by 28 · see citing works
Self-citationAlphavirus Encephalomyelitis: Mechanisms and Approaches to Prevention of Neuronal Damage
Griffin, D. E. (2016) · Neurotherapeutics · doi:10.1007/s13311-016-0434-6 · Cited by 25 · see citing works
Self-citationBaxter, V. K., Glowinski, R. M., Braxton, A. M., Potter, M. C., Slusher, B. S., & Griffin, D. E. (2017) · Virology · doi:10.1016/j.virol.2017.05.013 · Cited by 25 · see citing works
Self-citationInterleukin-10 Modulation of Virus Clearance and Disease in Mice with Alphaviral Encephalomyelitis
Martin, N., & Griffin, D. E. (2017) · Journal of Virology · doi:10.1128/jvi.01517-17 · Cited by 25 · see citing works
Self-citationGenetic control of alphavirus pathogenesis
Baxter, V. K., & Heise, M. T. (2018) · Mammalian Genome · doi:10.1007/s00335-018-9776-1 · Cited by 21 · see citing works
Self-citationModulating glutamine metabolism to control viral immuno-inflammatory lesions
Sumbria, D., Berber, E., Miller, L., & Rouse, B. T. (2021) · Cellular Immunology · doi:10.1016/j.cellimm.2021.104450 · Cited by 20 · see citing works
Inhibition of glutamine metabolism accelerates resolution of acute lung injury
Vigeland, C. L., Beggs, H. S., Collins, S. L., Chan‐Li, Y., Powell, J. D., Doerschuk, C. M., & Horton, M. R. (2019) · Physiological Reports · doi:10.14814/phy2.14019 · Cited by 20 · see citing works
Clark, I. A. (2022) · Pharmacology Research & Perspectives · doi:10.1002/prp2.926 · Cited by 18 · see citing works
Metabolic Pathways in Alloreactive T Cells
Brown, R., & Byersdorfer, C. A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01517 · Cited by 17 · see citing works
Therapeutic resurgence of 6-diazo-5-oxo-l-norleucine (DON) through tissue-targeted prodrugs
Novotná, K., Tenora, L., Slusher, B. S., & Rais, R. (2024) · Advances in pharmacology · doi:10.1016/bs.apha.2024.04.003 · Cited by 12 · see citing works
Self-citationBaxter, V. K., Troisi, E. M., Pate, N., Zhao, J. N., & Griffin, D. E. (2018) · Journal of General Virology · doi:10.1099/jgv.0.001005 · Cited by 10 · see citing works
Self-citationFongsaran, C., Jirakanwisal, K., Peng, B.-H., Fracassi, A., Taglialatela, G., Dineley, K. T., Paessler, S., & Cisneros, I. E. (2024) · Brain, Behavior, & Immunity - Health · doi:10.1016/j.bbih.2024.100780 · Cited by 9 · see citing works
Griffin, D. E. (2016) · Springer eBooks · doi:10.1007/978-3-319-33133-1_7 · Cited by 4 · see citing works
Self-citationClark, I. A. (2021) · International Journal for Parasitology · doi:10.1016/j.ijpara.2021.10.002 · Cited by 2 · see citing works
Williams, R. E., Pieterse, L., Patel, S. S., McLaren, M. W., Elrick, M. J., & Griffin, D. E. (2026) · Journal of Virology · doi:10.1128/jvi.00113-26 · Cited by 1 · see citing works
Self-citationLemberg, K. M., Zhao, L., Wu, Y., Veeravalli, V., Alt, J., Aguilar, J. M. H., Dash, R. P., Lam, J., Tenora, L., Rodriguez, C., et al. (2023) · doi:10.1158/1535-7163.c.6538519.v1
Self-citationWilliams, R. E., Pieterse, L., Patel, S. S., McLaren, M. L., Elrick, M. J., & Griffin, D. E. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.23.701280
Self-citationLantz, A., Green, F. M., Cowan, A., Miller, K. A., Saldivar, R. A., Anderson, E. J., Barre, R. S., Shivanna, V., Klimstra, W., Martínez-Sobrido, L., et al. (2026) · PLoS Pathogens · doi:10.1371/journal.ppat.1014395
Self-citationCusi, M. G., Savellini, G. G., Cassol, C., Nencioni, C., Bernini, L., Tacconi, D., Alessandri, G., Rizzo, L., Anichini, G., Smura, T., et al. (2026) · Emerging Microbes & Infections · doi:10.1080/22221751.2026.2703397
Opoku, L. A., Trefry, S. V., Konadu, M., Sanchez, J. O., Gomeiz, A., Walls, S. D., Barrera, M. D., Scarton, D. V., Veneziano, R., Pierobon, M., et al. (2026) · Microorganisms · doi:10.3390/microorganisms14091944
- Authors
- Potter, M. C., Baxter, V. K., Mathey, R. W., Alt, J., Rojas, C., Griffin, D. E., & Slusher, B. S.
- Affiliations
- Johns Hopkins University (US)
- Corresponding author
- Griffin, Diane E.
- Slusher, Barbara S.
- ORCID
- Venue
- Journal of NeuroVirology
- Published
- 2015-02-03
- Volume
- 21
- Issue
- 2
- Pages
- 159-173
- ISSN
- 1355-0284 (ISSN-L)
- 1538-2443
- PMC
- PMC4375032
- OpenAlex
- W1970803505
- Cited by
- 32
- References
- 65
- Citations by year
- 2026: 5 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 5 · 2020: 2 · 2019: 2 · 2018: 5 · 2017: 3 · 2016: 6
- FWCI
- 25.49
- Type
- book chapter
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of NeuroVirology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Johns Hopkins University
- National Institutes of Health (T32OD011089)
- National Institute of Mental Health (P30MH075673)
- National Institute on Drug Abuse (R03DA032470)
- National Institute of Neurological Disorders and Stroke (R01NS087539, R01NS038932)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
- Health Sciences › Medicine › Infectious Diseases › Infectious Encephalopathies and Encephalitis
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Sindbis virus, 6-diazo-5-oxo-L-norleucine, glutamine antagonist, neurocognitive impairment, hippocampal-dependent memory, glutamate excitotoxicity, neuroinflammation, inflammatory cell infiltration, neuroprotection, viral persistence, mouse model
- MeSH terms
- Animals, Antimetabolites, Antineoplastic, Behavior, Animal, Diazooxonorleucine, Disease Models, Animal, Enzyme-Linked Immunosorbent Assay, Glutamine, Immunohistochemistry, Male, Mice, Inbred C57BL, Motor Activity, Sindbis Virus, Alphavirus Infections, Encephalitis, Viral, Mice
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