Prion infection of mouse brain reveals multiple new upregulated genes involved in neuroinflammation or signal transduction

Carroll, James A.; Striebel, James F.; Race, Brent; Phillips, Katie; Chesebro, Bruce

doi:10.1128/jvi.02952-14

Cited by 63Prion Diseases and Protein MisfoldingNeuroinflammation and Neurodegeneration MechanismsAlzheimer's disease research and treatments

Prion infection of mouse brain reveals multiple new upregulated genes involved in neuroinflammation or signal transduction

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Carroll, James A., Striebel, James F., Race, Brent, Phillips, Katie, Chesebro, Bruce·2015·Journal of Virology

DOI 10.1128/jvi.02952-14PMC PMC4338885

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Abstract

Gliosis is often a preclinical pathological finding in neurodegenerative diseases, including prion diseases, but the mechanisms facilitating gliosis and neuronal damage in these diseases are not understood. To expand our knowledge of the neuroinflammatory response in prion diseases, we assessed the expression of key genes and proteins involved in the inflammatory response and signal transduction in mouse brain at various times after scrapie infection. In brains of scrapie-infected mice at pre- and postclinical stages, we identified 15 previously unreported differentially expressed genes related to inflammation or activation of the STAT signal transduction pathway. Levels for the majority of differentially expressed genes increased with time postinfection. In quantitative immunoblotting experiments of STAT proteins, STAT1α, phosphorylated-STAT1α (pSTAT1α), and pSTAT3 were increased between 94 and 131 days postinfection (p.i.) in brains of mice infected with strain 22L. Furthermore, a select group of STAT-associated genes was increased preclinically during scrapie infection, suggesting early activation of the STAT signal transduction pathway. Comparison of inflammatory markers between mice infected with scrapie strains 22L and RML indicated that the inflammatory responses and gene expression profiles in the brains were strikingly similar, even though these scrapie strains infect different brain regions. The endogenous interleukin-1 receptor antagonist (IL-1Ra), an inflammatory marker, was newly identified as increasing preclinically in our model and therefore might influence scrapie pathogenesis in vivo. However, in IL-1Ra-deficient or overexpressor transgenic mice inoculated with scrapie, neither loss nor overexpression of IL-1Ra demonstrated any observable effect on gliosis, protease-resistant prion protein (PrPres) formation, disease tempo, pathology, or expression of the inflammatory genes analyzed. IMPORTANCE Prion infection leads to PrPres deposition, gliosis, and neuroinflammation in the central nervous system before signs of clinical illness. Using a scrapie mouse model of prion disease to assess various time points postinoculation, we identified 15 unreported genes that were increased in the brains of scrapie-infected mice and were associated with inflammation and/or JAK-STAT activation. Comparison of mice infected with two scrapie strains (22L and RML), which have dissimilar neuropathologies, indicated that the inflammatory responses and gene expression profiles in the brains were similar. Genes that increased prior to clinical signs might be involved in controlling scrapie infection or in facilitating damage to host tissues. We tested the possible role of the endogenous IL-1Ra, which was increased at 70 days p.i. In scrapie-infected mice deficient in or overexpressing IL-1Ra, there was no observable effect on gliosis, PrPres formation, disease tempo, pathology, or expression of inflammatory genes analyzed.

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Several proinflammatory cytokines, including TNF α, IL 1α, and C1qa, are upregulated in the brain during the prion disease course.
“Several proinflammatory cytokines are upregulated in the brain during the prion disease course including TNF α, IL 1α, and C1qa [46,69,70,71,72,73].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [70]
Transcription of several genes encoding DAMP proteins and receptors such as Toll-like receptors or proteins of the complement cascade is increased in the brains of prion-infected mice.
“In addition to the upregulation of PAMPs in prion diseases, the transcription of several genes encoding damage-associated molecular pattern (DAMP) proteins and receptors such as Toll-like receptors or proteins of the complement cascade are also increased in the brains of prion-infected mice [70,82].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [70]

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
Towbin, H., Staehelin, T., & Gordon, J. (1979) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.76.9.4350 · Cited by 51,421 · see citing works
Short-Term Effects of Nose-Only Cigarette Smoke Exposure on Glutathione Redox Homeostasis, Cytochrome P450 1A1/2 and Respiratory Enzyme Activities in Mice Tissues
Raza, H., John, A., & Nemmar, A. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350087 · Cited by 47,311 · see citing works
A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples
Markwell, M. A. K., Haas, S. M., BIEBER, L. L., & Tolbert, N. E. (1978) · Analytical Biochemistry · doi:10.1016/0003-2697(78)90586-9 · Cited by 6,460 · see citing works
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
TRANCE Is a Novel Ligand of the Tumor Necrosis Factor Receptor Family That Activates c-Jun N-terminal Kinase in T Cells
Wong, B. R., Rho, J., Arron, J. R., Robinson, E. A., Orlinick, J. R., Chao, M. V., Kalachikov, S. M., Cayani, E., Bartlett, F. S., Frankel, W. N., et al. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.40.25190 · Cited by 1,042 · see citing works
Prion protein (PrP) with amino‐proximal deletions restoring susceptibility of PrP knockout mice to scrapie.
Fischer, M. B., Rülicke, T., Raeber, A. J., Sailer, A. W., Moser, M., Oesch, B., Brandner, S., Aguzzi, A., & Weissmann, C. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00467.x · Cited by 878 · see citing works
NF-κB and STAT3 signaling pathways collaboratively link inflammation to cancer
Fan, Y., Mao, R., & Yang, J. (2013) · Protein & Cell · doi:10.1007/s13238-013-2084-3 · Cited by 779 · see citing works
Persistently Activated Stat3 Maintains Constitutive NF-κB Activity in Tumors
Lee, H., Herrmann, A., Deng, J.-H., Kujawski, M., Niu, G., Li, Z., Forman, S., Jove, R., Pardoll, D. M., & Yu, H. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.02.015 · Cited by 683 · see citing works
Histone deacetylases, transcriptional control, and cancer
Cress, W. D., & Seto, E. (2000) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(200007)184:1 · Cited by 619 · see citing works
Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFκB
Yang, J., Liao, X., Agarwal, M. K., Barnes, L., Auron, P. E., & Stark, G. R. (2007) · Genes & Development · doi:10.1101/gad.1553707 · Cited by 611 · see citing works
Reliability and reproducibility issues in DNA microarray measurements
DRAGHICI, S., KHATRI, P., EKLUND, A., & SZALLASI, Z. (2006) · Trends in Genetics · doi:10.1016/j.tig.2005.12.005 · Cited by 590 · see citing works
Biological properties of recombinant human monocyte-derived interleukin 1 receptor antagonist.
Arend, W. P., Welgus, H. G., Thompson, R. C., & Eisenberg, S. P. (1990) · Journal of Clinical Investigation · doi:10.1172/jci114622 · Cited by 581 · see citing works
Biology and significance of the JAK/STAT signalling pathways
Kiu, H., & Nicholson, S. E. (2012) · Growth Factors · doi:10.3109/08977194.2012.660936 · Cited by 470 · see citing works
Neuropathological Diagnostic Criteria for Creutzfeldt‐Jakob Disease (CJD) and Other Human Spongiform Encephalopathies (Prion Diseases)
Budka, H., Aguzzi, A., Brown, P., Brucher, J., Bugiani, O., Gullotta, F., Haltia, M., Hauw, J., Ironside, J. W., Jellinger, K. A., et al. (1995) · Brain Pathology · doi:10.1111/j.1750-3639.1995.tb00625.x · Cited by 428 · see citing works
Synergy between Interferon-γ and Tumor Necrosis Factor-α in Transcriptional Activation Is Mediated by Cooperation between Signal Transducer and Activator of Transcription 1 and Nuclear Factor κB
Ohmori, Y., Schreiber, R. D., & Hamilton, T. A. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.23.14899 · Cited by 413 · see citing works
Isolation of glia from Alzheimer’s mice reveals inflammation and dysfunction
Orre, M., Kamphuis, W., Osborn, L. M., Jansen, A. H. P., Kooijman, L., Bossers, K., & Hol, E. M. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.06.004 · Cited by 394 · see citing works
The disease characteristics of different strains of scrapie in Sinc congenic mouse lines: implications for the nature of the agent and host control of pathogenesis
Bruce, M. E., McConnell, I., Fraser, H., & Dickinson, A. G. (1991) · Journal of General Virology · doi:10.1099/0022-1317-72-3-595 · Cited by 388 · see citing works
Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells
Oka, K., Sawamura, T., Kikuta, K., Itokawa, S., Kume, N., Kita, T., & Masaki, Τ. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.16.9535 · Cited by 383 · see citing works
Hepatic acute phase proteins – Regulation by IL-6- and IL-1-type cytokines involving STAT3 and its crosstalk with NF-κB-dependent signaling
Bode, J. G., Albrecht, U., Häussinger, D., Heinrich, P. C., & Schaper, F. (2012) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2011.09.008 · Cited by 379 · see citing works
Interleukin‐1: A master regulator of neuroinflammation
Basu, A., Krady, J. K., & Levison, S. W. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20266 · Cited by 367 · see citing works
Neurogenesis, inflammation and behavior
Kohman, R. A., & Rhodes, J. S. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.09.003 · Cited by 363 · see citing works
The role of JAK-STAT signaling within the CNS
Nicolas, C. S., Amici, M., Bortolotto, Z. A., Doherty, A. J., Csaba, Z., Fafouri, A., Dournaud, P., Gressèns, P., Collingridge, G. L., & Peineau, S. (2013) · JAK-STAT · doi:10.4161/jkst.22925 · Cited by 352 · see citing works
The MCP/eotaxin subfamily of CC chemokines
Coillie, E. V., Damme, J. V., & Opdenakker, G. (1999) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(99)00005-2 · Cited by 351 · see citing works
Functions of interleukin 1 receptor antagonist in gene knockout and overproducing mice.
Hirsch, E., Irikura, V. M., Paul, S. M., & Hirsh, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.20.11008 · Cited by 317 · see citing works
A systems approach to prion disease
Hwang, D., Lee, I. Y., Yoo, H., Gehlenborg, N., Cho, J., Petritis, B., Baxter, D., Pitstick, R., Young, R., Spicer, D., et al. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.10 · Cited by 287 · see citing works
New perspectives on central and peripheral immune responses to acute traumatic brain injury
Das, M., Mohapatra, S., & Mohapatra, S. S. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-236 · Cited by 282 · see citing works
Chemokines: attractive mediators of the immune response
Wong, M., & Fish, E. N. (2002) · Seminars in Immunology · doi:10.1016/s1044-5323(02)00123-9 · Cited by 268 · see citing works
Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie‐infected murine hippocampus
Jeffrey, M., Halliday, W. G., Bell, J. D., Johnston, A. R., MacLeod, N. K., Ingham, C. A., Sayers, A. R., Brown, D. A., & Fraser, J. R. (2000) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.2000.00216.x · Cited by 261 · see citing works
Signal transducers and activators of transcription 3 (STAT3) inhibits transcription of the inducible nitric oxide synthase gene by interacting with nuclear factor κB
YU, Z., ZHANG, W., & KONE, B. C. (2002) · Biochemical Journal · doi:10.1042/bj20020588 · Cited by 255 · see citing works
IL-12 production by central nervous system microglia is inhibited by astrocytes
Aloisi, F., Penna, G., Cerase, J., Iglesias, B. M., & Adorini, L. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.4.1604 · Cited by 252 · see citing works
Evidence that the Transmission of One Source of Scrapie Agent to Hamsters Involves Separation of Agent Strains from a Mixture
Kimberlin, R. H., & Walker, C. A. (1978) · Journal of General Virology · doi:10.1099/0022-1317-39-3-487 · Cited by 250 · see citing works
IFN-γ signaling, with the synergistic contribution of TNF-α, mediates cell specific microglial and astroglial activation in experimental models of Parkinson's disease
Barcia, C., Ros, C., Annese, V., Gómez, A., Ros-Bernal, F., Aguado-Yera, D., Martı́nez-Pagán, M., de Pablos, V., Fernández-Villalba, E., & Herrero, M. (2011) · Cell Death and Disease · doi:10.1038/cddis.2011.17 · Cited by 242 · see citing works
Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders
Keyser, J. D., Mostert, J. P., & Koch, M. W. (2007) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2007.08.044 · Cited by 235 · see citing works
The Genomic Identity of Different Strains of Mouse Scrapie Is Expressed in Hamsters and Preserved on Reisolation in Mice
Kimberlin, R. H., Walker, C. A., & Fraser, H. (1989) · Journal of General Virology · doi:10.1099/0022-1317-70-8-2017 · Cited by 222 · see citing works
The role of 2′-5′ oligoadenylate-activated ribonuclease L in apoptosis
Castelli, J. C., Hassel, B. A., Maran, A., Paranjape, J. M., Hewitt, J., Li, X.-L., Hsu, Y., Silverman, R. H., & Youle, R. J. (1998) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400352 · Cited by 181 · see citing works
Human immunodeficiency virus type 1 Nef protein mediates neural cell death: a neurotoxic role for IP-10
van Marle, G., Henry, S. D., Todoruk, T. R., Sullivan, A., Silva, C., Rourke, S. B., Holden, J. K., McArthur, J. C., Gill, M. J., & Power, C. (2004) · Virology · doi:10.1016/j.virol.2004.08.024 · Cited by 180 · see citing works
Neurotoxic effects of tumor necrosis factor alpha in primary human neuronal cultures are mediated by activation of the glutamate AMPA receptor subtype: implications for AIDS neuropathogenesis.
Gelbard, H., Dzenko, K., Diloreto, D., del Cerro, C., del Cerro, M. D., & Epstein, L. G. (1993) · Developmental Neuroscience · doi:10.1159/000111367 · Cited by 175 · see citing works
CXCL10‐induced cell death in neurons: role of calcium dysregulation
Sui, Y., Stehno‐Bittel, L., Li, S., Loganathan, R., Dhillon, N. K., Pinson, D. M., Nath, A., Kolson, D. L., Narayan, O., & Buch, S. J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04631.x · Cited by 173 · see citing works
Entry versus Blockade of Brain Infection following Oral or Intraperitoneal Scrapie Administration: Role of Prion Protein Expression in Peripheral Nerves and Spleen
Race, R., Oldstone, M. B. A., & Chesebro, B. W. (2000) · Journal of Virology · doi:10.1128/jvi.74.2.828-833.2000 · Cited by 170 · see citing works
Self-citation
Comparison of mRNA gene expression by RT-PCR and DNA microarray
Etienne, W., Meyer, M. H., Peppers, J., & Meyer, R. A. (2004) · BioTechniques · doi:10.2144/04364st02 · Cited by 168 · see citing works
Unique inflammatory RNA profiles of microglia in Creutzfeldt–Jakob disease
Baker, C. A., & Manuelidis, L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0237313100 · Cited by 165 · see citing works
RANTES and MIP-1α Activate Stats in T Cells
Wong, M., & Fish, E. N. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.1.309 · Cited by 157 · see citing works
Identification of Differentially Expressed Genes in Scrapie-Infected Mouse Brains by Using Global Gene Expression Technology
Xiang, W., Windl, O., Wünsch, G., Dugas, M., Kohlmann, A., Dierkes, N., Westner, I. M., & Kretzschmar, H. A. (2004) · Journal of Virology · doi:10.1128/jvi.78.20.11051-11060.2004 · Cited by 150 · see citing works
Tyk2/STAT3 Signaling Mediates β-Amyloid-Induced Neuronal Cell Death: Implications in Alzheimer's Disease
Wan, J., Fu, A. K. Y., Ip, F. C. F., Ng, H., Hugon, J., Page, G., Wang, J. H.-C., Lai, K., Wu, Z., & Ip, N. Y. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0519-10.2010 · Cited by 143 · see citing works
Scrapie Strain Variation and Its Implications
Bruce, M. E., & Fraser, H. (1991) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-76540-7_8 · Cited by 143 · see citing works
RANKL/RANK—beyond bones
Hanada, R., Hanada, T., Sigl, V., Schramek, D., & Penninger, J. M. (2011) · Journal of Molecular Medicine · doi:10.1007/s00109-011-0749-z · Cited by 139 · see citing works
Activation of cerebral cytokine gene expression and its correlation with onset of reactive astrocyte and acute-phase response gene expression in scrapie
Campbell, I. L., Eddleston, M., Kemper, P., Oldstone, M. B. A., & Hobbs, M. V. (1994) · Journal of Virology · doi:10.1128/jvi.68.4.2383-2387.1994 · Cited by 136 · see citing works
OPG/RANKL/RANK axis is a critical inflammatory signaling system in ischemic brain in mice
Shimamura, M., Nakagami, H., Osako, M. K., Kurinami, H., Koriyama, H., Zhengda, P., Tomioka, H., Tenma, A., Wakayama, K., & Morishita, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400544111 · Cited by 134 · see citing works
Paradoxical shortening of scrapie incubation times by expression of prion protein transgenes derived from long incubation period mice
Westaway, D. A., Mirenda, C. A., FOSTER, D. B., Zebarjadian, Y., Scott, M., Torchia, M., Yang, S.-L., Serban, H., DeArmond, S. J., Ebeling, C., et al. (1991) · Neuron · doi:10.1016/0896-6273(91)90074-a · Cited by 134 · see citing works
Immunocytochemical appearance of cytokines, prostaglandin E2 and lipocortin-1 in the CNS during the incubation period of murine scrapie correlates with progressive PrP accumulations
Williams, A., van Dam, A., Ritchie, D. L., Eikelenboom, P., & Fraser, H. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00067-x · Cited by 133 · see citing works
Classical sheep transmissible spongiform encephalopathies: pathogenesis, pathological phenotypes and clinical disease
Jeffrey, M., & González, L. (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00868.x · Cited by 128 · see citing works
Fatal Transmissible Amyloid Encephalopathy: A New Type of Prion Disease Associated with Lack of Prion Protein Membrane Anchoring
Chesebro, B. W., Race, B., Meade-White, K. D., LaCasse, R. A., Race, R., Klingeborn, M., Striebel, J. F., Dorward, D. W., McGovern, G., & Jeffrey, M. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000800 · Cited by 128 · see citing works
Self-citation
Expression of cytokine genes and increased nuclear factor-kappa B activity in the brains of scrapie-infected mice
Kim, J., Ju, W., Choi, J., Kim, J., Choi, E., Carp, R. I., Wı́sniewski, H. M., & Kim, Y. (1999) · Molecular Brain Research · doi:10.1016/s0169-328x(99)00229-6 · Cited by 120 · see citing works
Synergistic activation of intercellular adhesion molecule 1 (ICAM‐1) by TNF‐α and IFN‐γ is mediated by p65/p50 and p65/c‐Rel and interferon‐responsive factor Statlα (p91) that can be activated by both IFN‐γ and IFN‐α
Jahnke, A., & Johnson, J. P. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)01130-3 · Cited by 116 · see citing works
Interactions between TLR7 and TLR9 agonists and receptors regulate innate immune responses by astrocytes and microglia
Butchi, N. B., Du, M., & Peterson, K. E. (2010) · Glia · doi:10.1002/glia.20952 · Cited by 109 · see citing works
Gene expression profiling of scrapie-infected brain tissue
Riemer, C., Neidhold, S., Burwinkel, M., Schwarz, A., Schultz, J., Krätzschmar, J., Mönning, U., & Baier, M. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.08.124 · Cited by 108 · see citing works
The Transcriptional Coactivator CREB-binding Protein Cooperates with STAT1 and NF-κB for Synergistic Transcriptional Activation of the CXC Ligand 9/Monokine Induced by Interferon-γ Gene
Hiroi, M., & Ohmori, Y. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204544200 · Cited by 106 · see citing works
Role of interleukin-1 in prion disease-associated astrocyte activation.
Schultz, J., Schwarz, A., Neidhold, S., Burwinkel, M., Riemer, C., Simon, D., Kopf, M., Otto, M., & Baier, M. (2004) · American Journal of Pathology · doi:10.1016/s0002-9440(10)63331-7 · Cited by 101 · see citing works
Cytokines, prostaglandins and lipocortin-1 are present in the brains of scrapie-infected mice
Williams, A. E., van Dam, A., Man‐A‐Hing, W. K. H., BERKENBOSCH, F., Eikelenboom, P., & Fraser, H. (1994) · Brain Research · doi:10.1016/0006-8993(94)90480-4 · Cited by 99 · see citing works
α2-Macroglobulin in late-onset Alzheimer's disease
Kovacs, D. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00113-3 · Cited by 98 · see citing works
Identification of USP18 as an Important Regulator of the Susceptibility to IFN-α and Drug-Induced Apoptosis
Potu, H., Sgorbissa, A., & Brancolini, C. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-1942 · Cited by 97 · see citing works
Early Mechanisms of Pathobiology Are Revealed by Transcriptional Temporal Dynamics in Hippocampal CA1 Neurons of Prion Infected Mice
Majer, A., Medina, S. J., Niu, Y., Abrenica, B., Manguiat, K., Frost, K. L., Phillipson, C. S., Sorensen, D. L., & Booth, S. A. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003002 · Cited by 96 · see citing works
Microglia and chemokines in infectious diseases of the nervous system: views and reviews
Kielian, T. (2004) · Frontiers in bioscience · doi:10.2741/1266 · Cited by 94 · see citing works
Resistance to Chronic Wasting Disease in Transgenic Mice Expressing a Naturally Occurring Allelic Variant of Deer Prion Protein
Meade-White, K. D., Race, B., Trifilo, M. J., Bossers, A., Favara, C., LaCasse, R. A., Miller, M. W., WILLIAMS, E. S., Oldstone, M. B. A., Race, R., et al. (2007) · Journal of Virology · doi:10.1128/jvi.02762-06 · Cited by 88 · see citing works
Self-citation
Gene expression alterations in brains of mice infected with three strains of scrapie
Skinner, P. J., Abbassi, H., Chesebro, B. W., Race, R., Reilly, C., & Haase, A. T. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-114 · Cited by 85 · see citing works
Self-citation
Comprehensive transcriptional profiling of prion infection in mouse models reveals networks of responsive genes
Sorensen, G., Medina, S. J., Parchaliuk, D. L., Phillipson, C. S., Robertson, C., & Booth, S. A. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-114 · Cited by 84 · see citing works
Identification of central nervous system genes involved in the host response to the scrapie agent during preclinical and clinical infection
Booth, S., Bowman, C., Baumgartner, R., Sorensen, G., Robertson, C., Coulthart, M. B., Phillipson, C. S., & Somorjai, R. L. (2004) · Journal of General Virology · doi:10.1099/vir.0.80110-0 · Cited by 83 · see citing works
Prostaglandin E2Is a Novel Inducer of Oncostatin-M Expression in Macrophages and Microglia
Repovic, P., & Benveniste, E. N. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05334.2002 · Cited by 78 · see citing works
The STAT3 DNA-Binding Domain Mediates Interaction with NF-κB p65 and Inducible Nitric Oxide Synthase Transrepression in Mesangial Cells
Yu, Z., & Kone, B. C. (2004) · Journal of the American Society of Nephrology · doi:10.1097/01.asn.0000114556.19556.f9 · Cited by 71 · see citing works
Analysis of Protein Levels of 24 Cytokines in Scrapie Agent-Infected Brain and Glial Cell Cultures from Mice Differing in Prion Protein Expression Levels
Tribouillard‐Tanvier, D., Striebel, J. F., Peterson, K. E., & Chesebro, B. W. (2009) · Journal of Virology · doi:10.1128/jvi.01413-09 · Cited by 68 · see citing works
Self-citation
Erratum: IFN-γ signaling, with the synergistic contribution of TNF-α, mediates cell specific microglial and astroglial activation in experimental models of Parkinson’s disease
Barcia, C., Ros, C. M., Annese, V., Gómez, A. M., Ros‐Bernal, F., Aguado‐Llera, D., Martínez-Pagán, M. E., de Pablos, V., Fernández‐Villalba, E., & Herrero, M. T. (2012) · Cell Death and Disease · doi:10.1038/cddis.2012.123 · Cited by 67 · see citing works
NF-κB and STAT3 signaling hubs for lung innate immunity
Quinton, L. J., & Mizgerd, J. P. (2011) · Cell and Tissue Research · doi:10.1007/s00441-010-1044-y · Cited by 65 · see citing works
Immune System in the Brain: A Modulatory Role on Dendritic Spine Morphophysiology?
Bitzer-Quintero, O. K., & González‐Burgos, I. (2012) · Neural Plasticity · doi:10.1155/2012/348642 · Cited by 63 · see citing works
Interactions Between TLR7 and TLR9 Agonists and Receptors Regulate Innate Immune Responses by Astrocytes and Microglia
Niranjan, Butchi, Min, Du, Karin, & Peterson (2010) · Acta Scientiarum Naturalium Universitatis Sunyatseni · Cited by 63 · see citing works
Onset of Accumulation of PrPresin Murine ME7 Scrapie in Relation to Pathological and PrP Immunohistochemical Changes
Jeffrey, M., Мартин, С., Barr, J., Chong, A., & Fraser, J. R. (2001) · Journal of Comparative Pathology · doi:10.1053/jcpa.2000.0423 · Cited by 58 · see citing works
Regulation of RANTES/CCL5 expression in human astrocytes by interleukin‐1 and interferon‐β
Kim, M., Suh, H.-S., Brosnan, C. F., & Lee, S. C. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02487.x · Cited by 58 · see citing works
Interleukin-1 receptor antagonist exerts agonist activity in the hippocampus independent of the interleukin-1 type I receptor
Loscher, C. E., Mills, K. H. G., & Lynch, M. A. (2003) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(03)00072-9 · Cited by 54 · see citing works
Comparison of Inflammatory and Acute-Phase Responses in the Brain and Peripheral Organs of the ME7 Model of Prion Disease
Cunningham, C. M., Wilcockson, D. C., Boche, D., & Perry, V. H. (2005) · Journal of Virology · doi:10.1128/jvi.79.8.5174-5184.2005 · Cited by 53 · see citing works
JAK‐STAT signaling pathway mediates astrogliosis in brains of scrapie‐infected mice
Na, Y., Jin, J., Kim, J., Choi, E., Carp, R. I., & Kim, Y. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04769.x · Cited by 50 · see citing works
Prion Protein Expression Differences in Microglia and Astroglia Influence Scrapie-Induced Neurodegeneration in the Retina and Brain of Transgenic Mice
Kercher, L., Favara, C., Striebel, J. F., LaCasse, R. A., & Chesebro, B. W. (2007) · Journal of Virology · doi:10.1128/jvi.00865-07 · Cited by 47 · see citing works
Self-citation
Expression of Concern: Gene expression profile activated by the chemokine CCL5/RANTES in human neuronal cells
Valerio, A., Ferrario, M., Martínez, F. O., Locati, M., Ghisi, V., Bresciani, L. G., Mantovani, A., & Spano, P. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20250 · Cited by 43 · see citing works
Inducible cytokine gene expression in the brain in the ME7/CV mouse model of scrapie is highly restricted, is at a strikingly low level relative to the degree of gliosis and occurs only late in disease
Brown, A. R., Webb, J., Rebus, S., WALKER, R. E., Williams, A., & Fazakerley, J. K. (2003) · Journal of General Virology · doi:10.1099/vir.0.19137-0 · Cited by 43 · see citing works
Gene regulatory network analysis supports inflammation as a key neurodegeneration process in prion disease
Crespo, I., Roomp, K., Jurkowski, W., Kitano, H., & del Sol, A. (2012) · BMC Systems Biology · doi:10.1186/1752-0509-6-132 · Cited by 41 · see citing works
Distinct patterns of spread of prion infection in brains of mice expressing anchorless or anchored forms of prion protein
Rangel, A., Race, B., Phillips, K. L., Striebel, J. F., Kurtz, N., & Chesebro, B. W. (2014) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-2-8 · Cited by 39 · see citing works
Self-citation
Evidence for Biological and Structural Diversity Among Scrapie Strains
Kascsak, R., Rubenstein, R., & Carp, R. I. (1991) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-76540-7_9 · Cited by 38 · see citing works
Identification of up‐regulated genes by array analysis in scrapie‐infected mouse brains
Brown, A. R., Webb, J., Rebus, S., Williams, A., & Fazakerley, J. K. (2004) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2004.00565.x · Cited by 37 · see citing works
Bindarit, Inhibitor of CCL2 Synthesis, Protects Neurons Against Amyloid-β-Induced Toxicity
Severini, C., Passeri, P. P., Ciotti, M. T., Florenzano, F., Possenti, R., Zona, C., Matteo, A. D., Guglielmotti, A., Calissano, P., Pachter, J. S., et al. (2013) · Journal of Alzheimer s Disease · doi:10.3233/jad-131070 · Cited by 36 · see citing works
Early Cytokine Elevation, PrPres Deposition, and Gliosis in Mouse Scrapie: No Effect on Disease by Deletion of Cytokine Genes IL-12p40 and IL-12p35
Tribouillard‐Tanvier, D., Race, B., Striebel, J. F., Carroll, J. A., Phillips, K. L., & Chesebro, B. W. (2012) · Journal of Virology · doi:10.1128/jvi.01340-12 · Cited by 36 · see citing works
Self-citation
The new role of LOX-1 in hypertension induced neuronal apoptosis
Li, Y., Duan, Z.-M., Gao, D., Huang, S., Yuan, H., & Niu, X. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.07.143 · Cited by 30 · see citing works
Role of Cyclophilin A from Brains of Prion-infected Mice in Stimulation of Cytokine Release by Microglia and Astroglia in Vitro
Tribouillard‐Tanvier, D., Carroll, J. A., Moore, R. A., Striebel, J. F., & Chesebro, B. W. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.269480 · Cited by 28 · see citing works
Self-citation
Presence of an acute phase response in sheep with clinical classical scrapie
Meling, S., Bårdsen, K., & Ulvund, M. J. (2012) · BMC Veterinary Research · doi:10.1186/1746-6148-8-113 · Cited by 27 · see citing works
STAT3/NFκB Interplay in the Regulation of α2‐Macroglobulin Gene Expression During Rat Liver Development and the Acute Phase Response
Uskoković, A. S., Dinić, S., Mihailović, M., Grigorov, I., Ivanović‐Matić, S., Bogojević, D., Grdović, N., Јovanović, J. A., Vidaković, M., Martinović, V., et al. (2007) · IUBMB Life · doi:10.1080/15216540701272612 · Cited by 25 · see citing works
Oncostatin M regulates neural precursor activity in the adult brain
Beatus, P., Jhaveri, D. J., Walker, T. L., Lucas, P. G., Rietze, R. L., Cooper, H. M., Morikawa, Y., & Bartlett, P. F. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20871 · Cited by 24 · see citing works
Prion disease induced alterations in gene expression in spleen and brain prior to clinical symptoms
Skinner, P. J. (2008) · Advances and Applications in Bioinformatics and Chemistry · doi:10.2147/aabc.s3411 · Cited by 23 · see citing works
Monocyte recruitment into the scrapie-affected brain
Williams, A. E., Ryder, S., & Blakemore, W. F. (1995) · Acta Neuropathologica · doi:10.1007/bf00294316 · Cited by 23 · see citing works
Activated α2Macroglobulin Increases β-Amyloid (25–35)-Induced Toxicity in LAN5 Human Neuroblastoma Cells
Fabrizi, C., Businaro, R., Lauro, G. M., Starace, G., & Fumagalli, L. (1999) · Experimental Neurology · doi:10.1006/exnr.1998.6978 · Cited by 22 · see citing works
Oncostatin M synergistically induces CXCL10 and ICAM‐1 expression in IL‐1β‐stimulated‐human gingival fibroblasts
Hosokawa, Y., Hosokawa, I., Ozaki, K., Nakae, H., & Matsuo, T. (2010) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22648 · Cited by 19 · see citing works
Upregulation Of Interferon-Gamma-Induced Genes During Prion Infection
Moody, L. R., Herbst, A. J., & Aiken, J. M. (2011) · Journal of Toxicology and Environmental Health · doi:10.1080/15287394.2011.529064 · Cited by 7 · see citing works

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RETRACTED: Neuroinflammatory Markers: Key Indicators in the Pathology of Neurodegenerative Diseases
Rauf, A., Badoni, H., Abu-Izneid, T., Olatunde, A., Rahman, M., Painuli, S., Semwal, P., Wilairatana, P., & Mubarak, M. (2022) · Molecules · doi:10.3390/molecules27103194 · Cited by 273 · see citing works
Retracted
Prion Strain Differences in Accumulation of PrPSc on Neurons and Glia Are Associated with Similar Expression Profiles of Neuroinflammatory Genes: Comparison of Three Prion Strains
Carroll, J. A., Striebel, J. F., Rangel, A., Woods, T., Phillips, K., Peterson, K. E., Race, B., & Chesebro, B. (2016) · PLOS Pathogens · doi:10.1371/journal.ppat.1005551 · Cited by 92 · see citing works
Self-citation
Microglia Are Critical in Host Defense against Prion Disease
Carroll, J. A., Race, B., Williams, K., Striebel, J., & Chesebro, B. (2018) · Journal of Virology · doi:10.1128/jvi.00549-18 · Cited by 94 · see citing works
Self-citation
Neuroinflammation, Microglia, and Cell-Association during Prion Disease
Carroll, J. A., & Chesebro, B. W. (2019) · Viruses · doi:10.3390/v11010065 · Cited by 82 · see citing works
Self-citation
Region-specific glial homeostatic signature in prion diseases is replaced by a uniform neuroinflammation signature, common for brain regions and prion strains with different cell tropism
Makarava, N., Chang, J. C.-Y., Molesworth, K., & Baskakov, I. V. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104783 · Cited by 64 · see citing works
She Doesn’t Even Go Here: The Role of Inflammatory Astrocytes in CNS Disorders
Reid, J. K., & Kuipers, H. F. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.704884 · Cited by 60 · see citing works
The Role of Microglia in Prion Diseases: A Paradigm of Functional Diversity
Obst, J., Simon, E., Mancuso, R., & Gómez‐Nicola, D. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00207 · Cited by 59 · see citing works
Neuropathology of Animal Prion Diseases
Orge, L., Lima, C., Machado, C., Tavares, P., Mendonça, P., Carvalho, P., Silva, J. P. N., Pinto, M. D. L., Bastos, E., Pereira, J. C., et al. (2021) · Biomolecules · doi:10.3390/biom11030466 · Cited by 51 · see citing works
Astrocyte-specific overexpressed gene signatures in response to methamphetamine exposure in vitro
Bortell, N., Basova, L. V., Semenova, S., Fox, H. S., Ravasi, T., & Marcondes, M. C. G. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0825-6 · Cited by 42 · see citing works
The molecular processes underpinning prion-like spreading and seed amplification in protein aggregation
Meisl, G., Knowles, T. P. J., & Klenerman, D. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.01.010 · Cited by 37 · see citing works
Oxidative and Inflammatory Events in Prion Diseases: Can They Be Therapeutic Targets?
Prasad, K. N., & Bondy, S. C. (2019) · Current Aging Science · doi:10.2174/1874609812666190111100205 · Cited by 32 · see citing works
RNA editing alterations define manifestation of prion diseases
Kanata, Ε., Llorens, F., Dafou, D., Dimitriadis, A., Thüne, K., Xanthopoulos, K., Bekas, N., Espinosa, J. C., Schmitz, M., Marín‐Moreno, A., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803521116 · Cited by 32 · see citing works
Regional and subtype-dependent miRNA signatures in sporadic Creutzfeldt-Jakob disease are accompanied by alterations in miRNA silencing machinery and biogenesis
Llorens, F., Thüne, K., Martı́, E., Kanata, Ε., Dafou, D., Lucena, D. D., Vivancos, A. P., Shomroni, O., Zafar, S., Schmitz, M., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1006802 · Cited by 32 · see citing works
microRNA-146a-5p, Neurotropic Viral Infection and Prion Disease (PrD)
Pogue, A. I., & Lukiw, W. J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179198 · Cited by 29 · see citing works
Increased Infectivity of Anchorless Mouse Scrapie Prions in Transgenic Mice Overexpressing Human Prion Protein
Race, B., Phillips, K. L., Meade-White, K. D., Striebel, J. F., & Chesebro, B. W. (2015) · Journal of Virology · doi:10.1128/jvi.00362-15 · Cited by 28 · see citing works
Self-citation
The cell type resolved mouse transcriptome in neuron-enriched brain tissues from the hippocampus and cerebellum during prion disease
Majer, A., Medina, S. J., Sorensen, D., Martin, M. J., Frost, K. L., Phillipson, C. S., Manguiat, K., & Booth, S. A. (2019) · Scientific Reports · doi:10.1038/s41598-018-37715-z · Cited by 26 · see citing works
MicroRNA Alterations in the Brain and Body Fluids of Humans and Animal Prion Disease Models: Current Status and Perspectives
Kanata, Ε., Thüne, K., Xanthopoulos, K., Ferrer, I., Dafou, D., Zerr, I., Sklaviadis, T., & Llorens, F. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00220 · Cited by 25 · see citing works
Redox stress and metal dys-homeostasis appear as hallmarks of early prion disease pathogenesis in mice
Spiers, J. G., Chen, H. C., Barry, T. L., Bourgognon, J.-M., & Steinert, J. R. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.09.025 · Cited by 24 · see citing works
Toll-like receptor 2 confers partial neuroprotection during prion disease
Carroll, J. A., Race, B., Williams, K., & Chesebro, B. (2018) · PLOS ONE · doi:10.1371/journal.pone.0208559 · Cited by 22 · see citing works
Self-citation
Statins are ineffective at reducing neuroinflammation or prolonging survival in scrapie-infected mice
Carroll, J. A., Race, B., Phillips, K. L., Striebel, J. F., & Chesebro, B. W. (2017) · Journal of General Virology · doi:10.1099/jgv.0.000876 · Cited by 23 · see citing works
Self-citation
Core transcriptional regulatory circuits in prion diseases
Kim, T., Lee, I., Cho, J.-H., Canine, B., Keller, A., Price, N. D., Hwang, D., Carlson, G. A., & Hood, L. (2020) · Molecular Brain · doi:10.1186/s13041-020-0551-3 · Cited by 20 · see citing works
Cerebellar compartmentation of prion pathogenesis
Ragagnin, A., Ezpeleta, J., Guillemain, A., Boudet-Devaud, F., Haeberlé, A., Demais, V., Vidal, C., Demuth, S., Béringue, V., Kellermann, O., et al. (2017) · Brain Pathology · doi:10.1111/bpa.12503 · Cited by 18 · see citing works
Transcriptomic Determinants of Scrapie Prion Propagation in Cultured Ovine Microglia
Muñoz-Gutiérrez, J. F., Pierlé, S. A., Schneider, D. A., Baszler, T. V., & Stanton, J. B. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147727 · Cited by 18 · see citing works
Loss of prion protein induces a primed state of type I interferon-responsive genes
Malachin, G., Reiten, M. R., Salvesen, Ø., Aanes, H., Kamstra, J. H., Skovgaard, K., Heegaard, P. M. H., Ersdal, C., Espenes, A., Tranulis, M. A., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0179881 · Cited by 18 · see citing works
Metal homeostasis disturbances in neurodegenerative disorders, with special emphasis on Creutzfeldt-Jakob disease – Potential pathogenetic mechanism and therapeutic implications
Nakagawa, Y., & Yamada, S. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107455 · Cited by 17 · see citing works
The role of the immune system in prion infection
Mabbott, N. A., Alibhai, J. D., & Manson, J. C. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63945-5.00005-2 · Cited by 17 · see citing works
Innate immune responses after stimulation with Toll-like receptor agonists in ex vivo microglial cultures and an in vivo model using mice with reduced microglia
Carroll, J. A., Race, B., Williams, K., Striebel, J. F., & Chesebro, B. W. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02240-w · Cited by 17 · see citing works
Self-citation
Loss of Homeostatic Microglia Signature in Prion Diseases
Wang, Y., Hartmann, K., Thies, E., Mohammadi, B., Altmeppen, H., Sepulveda-Falla, D., Glatzel, M., & Krasemann, S. (2022) · Cells · doi:10.3390/cells11192948 · Cited by 12 · see citing works
“In addition to the upregulation of PAMPs in prion diseases, the transcription of several genes encoding damage-associated molecular pattern (DAMP) proteins and receptors such as Toll-like receptors or proteins of the complement cascade are also increased in the brains of prion-infected mice [70,82].”
Background
Regional Differences in Neuroinflammation-Associated Gene Expression in the Brain of Sporadic Creutzfeldt–Jakob Disease Patients
Areškevičiūtė, A., Litman, T., Broholm, H., Melchior, L. C., Nielsen, P. R., Green, A., Eriksen, J. O., Smith, C., & Lund, E. L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010140 · Cited by 13 · see citing works
Immunology of Prion Protein and Prions
Mabbott, N. A. (2017) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2017.06.004 · Cited by 539 · see citing works
Prion Diseases
Whitechurch, B. C., Welton, J. M., Collins, S. J., & Lawson, V. (2017) · Advances in neurobiology · doi:10.1007/978-3-319-57193-5_13 · Cited by 13 · see citing works
Microglia-specific NF-κB signaling is a critical regulator of prion-induced glial inflammation and neuronal loss
Hay, A. J. D., Popichak, K. A., Mumford, G., Shirley, P. M., Bian, J., Wolfrath, L., Lei, S., Eggers, M., Nicholson, E. M., Tjalkens, R. B., et al. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1012582 · Cited by 10 · see citing works
Transcriptomic responses to prion disease in rats
Herbst, A. J., Ness, A., Johnson, C. J., McKenzie, D. I., & Aiken, J. M. (2015) · BMC Genomics · doi:10.1186/s12864-015-1884-7 · Cited by 10 · see citing works
Prions and prion diseases: Insights from the eye
Singh, N., Chaudhary, S., Ashok, A., & Lindner, E. (2020) · Experimental Eye Research · doi:10.1016/j.exer.2020.108200 · Cited by 10 · see citing works
Biological characteristics and transcriptomic profile of adipose-derived mesenchymal stem cells isolated from prion-infected murine model
Zayed, M., Kim, Y., & Jeong, B. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04273-x · Cited by 9 · see citing works
Adipose-derived mesenchymal stromal cells decrease prion-induced glial inflammation in vitro
Hay, A. J. D., Murphy, T. J., Popichak, K. A., Zabel, M. D., & Moreno, J. A. (2022) · Scientific Reports · doi:10.1038/s41598-022-26628-7 · Cited by 11 · see citing works
The impact of self-replicating proteins on inflammation, autoimmunity and neurodegeneration—An untraveled path
Butnaru, D., & Chapman, J. (2019) · Autoimmunity Reviews · doi:10.1016/j.autrev.2018.09.009 · Cited by 9 · see citing works
Redox mechanisms and their pathological role in prion diseases: The road to ruin
Spiers, J. G., Chen, H. C., & Steinert, J. R. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011309 · Cited by 8 · see citing works
Upregulation of brain hepcidin in prion diseases
Chaudhary, S., Ashok, A., Wise, A. S., Rana, N. A., McDonald, D., Kritikos, A. E., Kong, Q., & Singh, N. (2021) · Prion · doi:10.1080/19336896.2021.1946377 · Cited by 8 · see citing works
Microglia have limited influence on early prion pathogenesis, clearance, or replication
Race, B., Williams, K., Baune, C., Striebel, J. F., Long, D., Thomas, T., Lubke, L. L., Chesebro, B. W., & Carroll, J. A. (2022) · PLoS ONE · doi:10.1371/journal.pone.0276850 · Cited by 7 · see citing works
Self-citation
In Situ Temporospatial Characterization of the Glial Response to Prion Infection
Michael, A. V., Greenlee, J. J., Harm, T. A., Moore, S. J., Zhang, M., Lind, M. S., Greenlee, M. H. W., & Smith, J. D. (2019) · Veterinary Pathology · doi:10.1177/0300985819861708 · Cited by 6 · see citing works
Cross-Linking Cellular Prion Protein Induces Neuronal Type 2-Like Hypersensitivity
Adhikari, U. K., Sakiz, E., Zhou, X., Habiba, U., Kumar, S., Mikhael, M., Senesi, M., Li, C. G., Guillemin, G. J., Ooi, L., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.639008 · Cited by 6 · see citing works
microRNA-146a as a biomarker for transmissible spongiform encephalopathy
Pogue, A. I., Zhao, Y., & Lukiw, W. J. (2022) · Folia Neuropathologica · doi:10.5114/fn.2022.113561 · Cited by 6 · see citing works
5-Methylcytosine and 5-Hydroxymethylcytosine in Scrapie-Infected Sheep and Mouse Brain Tissues
Hernaiz, A., Sentre, S., Betancor, M., López-Pérez, Ó., Salinas‐Pena, M., Zaragoza, P., Badiola, J. J., Toivonen, J. M., Bolea, R., & Martín‐Burriel, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021621 · Cited by 5 · see citing works
The Role of Glial Cells in Neurobiology and Prion Neuropathology
Hay, A. J. D., Popichak, K. A., Moreno, J. A., & Zabel, M. D. (2024) · Cells · doi:10.3390/cells13100832 · Cited by 5 · see citing works
Neuroimmune Response Mediated by Cytokines in Natural Scrapie after Chronic Dexamethasone Treatment
Guijarro, I. M., Garcés, M., Andrés‐Benito, P., Marín, B., Otero, A., Barrio, T., Carmona, M., Ferrer, I., Badiola, J. J., & Monzón, M. (2021) · Biomolecules · doi:10.3390/biom11020204 · Cited by 5 · see citing works
Omics of Prion Diseases
Vanni, S. (2017) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2017.05.004 · Cited by 5 · see citing works
Neuroimmune Response in Natural Preclinical Scrapie after Dexamethasone Treatment
Guijarro, I. M., Garcés, M., Marín, B., Otero, A., Barrio, T., Badiola, J. J., & Monzón, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165779 · Cited by 5 · see citing works
The ME7 prion model of neurodegeneration as a tool to understand and target neuroinflammation in Alzheimer’s disease
Chouhan, J. K., Fowler, S. A., Webster, C. I., & Teeling, J. L. (2017) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2018.10.004 · Cited by 4 · see citing works
Effect of Microglial Inflammation in Prion Disease
Ano, Y., Sakudo, A., & Onodera, T. (2019) · Current Issues in Molecular Biology · doi:10.21775/cimb.036.001 · Cited by 4 · see citing works
Neuroinflammation and Oxidative Stress in Models of Parkinson’s Disease and Protein-Misfolding Disorders
Tjalkens, R. B., Streifel, K. M., & Moreno, J. A. (2017) · Royal Society of Chemistry eBooks · doi:10.1039/9781782622888-00184 · Cited by 2 · see citing works
Oligoadenylate synthetase 1a suppresses prion infection through binding to cellular prion protein
Homma, T., Nakagaki, T., Nishinakagawa, T., Morita, Y., Atarashi, R., Kakuta, S., Iwakura, Y., Nishida, N., & Ishibashi, D. (2025) · Brain · doi:10.1093/brain/awaf193 · Cited by 2 · see citing works
CD11c is not required by microglia to convey neuroprotection after prion infection
Carroll, J. A., Striebel, J. F., Baune, C., Chesebro, B. W., & Race, B. (2023) · PLoS ONE · doi:10.1371/journal.pone.0293301 · Cited by 2 · see citing works
Self-citation
Rapidly Progressive Dementia After Platelet-Rich Plasma Therapy: A Case of Sporadic Creutzfeldt-Jakob Disease in the Context of Chronic Ehrlichiosis
Dave, M., & Le, P. (2025) · Cureus · doi:10.7759/cureus.91152 · Cited by 1 · see citing works
Loss of region-specific glial homeostatic signature in prion diseasesPreprint
Makarava, N., Chang, J. C., Molesworth, K., & Baskakov, I. V. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.21203/rs.2.17016/v1 · Cited by 1 · see citing works
Effect of Microglial Inflammation in Prion Disease
Ano, Y., Sakudo, A., & Onodera, T. (2018) · Caister Academic Press eBooks · doi:10.21775/9781910190951.03
Panoply of plant extracts in the treatment of prion diseases
Obulesu, M. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-95762-5.00002-3
In situ assessment of neuroinflammatory cytokines in different stages of ovine natural prion disease
Guijarro, I. M., Garcés, M., Badiola, J. J., & Monzón, M. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1404770
Role of Enzymes in Prion Disease: A Molecular Mechanism
Firdous, S. M., Pal, S., & Mandal, S. (2024) · Springer eBooks · doi:10.1007/978-981-97-6822-6_8
Metabolic and Inflammatory Stimuli Impact Vascular Circulation and Cell Proliferation Processes in the Amygdala
Bhamidi, S., Sunderland, G. R., Southey, B. R., Villamil, M. B., Johnson, R. W., & Rodriguez‐Zas, S. L. (2025) · Genes Brain & Behavior · doi:10.1111/gbb.70036
La protéine prion cellulaire : un relai de neurotoxicité commun aux protéines amyloïdes et aux nanoparticules
Boudet-Devaud, F. (2018) · theses.fr (ABES) · doi:10.70675/111341b9z5eeez4531z8f07zcb44d6f469a0
Du rôle physiologique de la protéine prion cellulaire à l'infection par les prions : régulation/dérégulation du module de signalisation PDK1/TACE α-secrétase
Ezpeleta, J. (2019) · doi:10.70675/4e7ccce5z4f1ez4a57zac28z5380a39dd820
Ubiquitin C-hydrolase L1 as a cerebrospinal fluid and blood biomarker for prion diseases
Canaslan, S., Schmitz, M., Fischer, A.-L., Correia, S., Correia, A. D. S., Saleem, T., Hermann, P., & Zerr, I. (2026) · Brain Communications · doi:10.1093/braincomms/fcag363

Comprehensive transcriptional profiling of prion infection in mouse models reveals networks of responsive genes
Sorensen, G., Medina, S. J., Parchaliuk, D. L., Phillipson, C. S., Robertson, C., & Booth, S. A. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-114 · Cited by 84 · see citing works
Early Cytokine Elevation, PrPres Deposition, and Gliosis in Mouse Scrapie: No Effect on Disease by Deletion of Cytokine Genes IL-12p40 and IL-12p35
Tribouillard‐Tanvier, D., Race, B., Striebel, J. F., Carroll, J. A., Phillips, K. L., & Chesebro, B. W. (2012) · Journal of Virology · doi:10.1128/jvi.01340-12 · Cited by 36 · see citing works
Self-citation
P4–125: JAK–STAT signaling pathway mediates astrogliosis in brains of scrapie–infected mice
Na, Y., Jin, J., Kim, J., Carp, R. I., & Kim, Y.-S. (2006) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2006.05.1864
Expression of cytokine genes and increased nuclear factor-kappa B activity in the brains of scrapie-infected mice
Kim, J., Ju, W., Choi, J., Kim, J., Choi, E., Carp, R. I., Wı́sniewski, H. M., & Kim, Y. (1999) · Molecular Brain Research · doi:10.1016/s0169-328x(99)00229-6 · Cited by 120 · see citing works
Identification of Differentially Expressed Genes in Scrapie-Infected Mouse Brains by Using Global Gene Expression Technology
Xiang, W., Windl, O., Wünsch, G., Dugas, M., Kohlmann, A., Dierkes, N., Westner, I. M., & Kretzschmar, H. A. (2004) · Journal of Virology · doi:10.1128/jvi.78.20.11051-11060.2004 · Cited by 150 · see citing works

Authors: Carroll, J. A., Striebel, J. F., Race, B., Phillips, K., & Chesebro, B.
Affiliations: National Institutes of Health (US)
ORCID: Carroll, James A.
Striebel, James F.
Race, Brent
Venue: Journal of Virology
Publisher: American Society for Microbiology
Published: 2015-02-15
Volume: 89
Issue: 4
Pages: 2388-2404
ISSN: 0022-538X (ISSN-L)
1098-5514
DOI: 10.1128/jvi.02952-14
PMC: PMC4338885
OpenAlex: W2095989144
Cited by: 63
References: 99
Citations by year: 2026: 1 · 2025: 5 · 2024: 3 · 2023: 3 · 2022: 7 · 2021: 7 · 2020: 6 · 2019: 10 · 2018: 7 · 2017: 10 · 2016: 2 · 2015: 2
FWCI: 1.91
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Virology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Allergy and Infectious Diseases
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Prion Diseases and Protein Misfolding
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Keywords: prion disease, scrapie, neuroinflammation, gliosis, JAK/STAT signaling, STAT1, STAT3, interleukin-1 receptor antagonist, differentially expressed genes, protease-resistant prion protein, gene expression profiling
MeSH terms: Animals, Brain, Disease Models, Animal, Female, Gliosis, Inflammation, Mice, Inbred C57BL, Mice, Transgenic, Scrapie, Signal Transduction, Neurodegenerative Diseases, Gene Expression Profiling

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Prion infection of mouse brain reveals multiple new upregulated genes involved in neuroinflammation or signal transduction

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