Interactions between TLR7 and TLR9 agonists and receptors regulate innate immune responses by astrocytes and microglia

Butchi, Niranjan B.; Du, Min; Peterson, Karin E.

doi:10.1002/glia.20952

Cited by 109Immune Response and InflammationNeuroinflammation and Neurodegeneration MechanismsInflammasome and immune disorders

Interactions between TLR7 and TLR9 agonists and receptors regulate innate immune responses by astrocytes and microglia

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Butchi, Niranjan B., Du, Min, Peterson, Karin E.·2010·Glia

DOI 10.1002/glia.20952PMC PMC3767435

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Abstract

Toll‐like receptors 7 (TLR7) and 9 (TLR9) are important mediators of innate immune responses. Both receptors are located in endosomal compartments, recognize nucleic acids, and signal via Myeloid differentiation factor 88 (MyD88). In the current study, we analyzed TLR7 and TLR9 induced activation of astrocytes and microglia, two cell types that contribute to innate immune responses in the CNS. TLR7 and TLR9 agonists induced similar cytokine profiles within each cell type. However, there were notable differences in the cytokine profile between astrocytes and microglia, including the production of the anti‐inflammatory cytokine IL‐10 and antiapoptotic cytokines G‐CSF and IL‐9 by microglia but not astrocytes. Costimulation studies demonstrated that the TLR7 agonist, imiquimod, could inhibit TLR9 agonist‐induced innate immune responses, in both cell types, in a concentration‐dependent manner. Surprisingly, this inhibition was not mediated by TLR7, as deficiency in TLR7 did not alter suppression of the TLR9 agonist‐induced responses. The suppression of innate immune responses was also not due to an inhibition of TLR9 agonist uptake. This suggested that imiquimod suppression may be a direct effect, possibly by blocking CpG‐ODN binding and/or signaling with TLR9, thus limiting cell activation. An antagonistic relationship was also observed between the two receptors in microglia, with TLR7 deficiency resulting in enhanced cytokine responses to CpG‐ODN stimulation. Thus, both TLR7 and its agonist can have inhibitory effects on TLR9‐induced cytokine responses in glial cells. © 2009 Wiley‐Liss, Inc.

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All of the AAV-induced cytokines and chemokines can be upregulated by activation of TLR9 in the periphery using synthetic CpG-rich oligonucleotides.
“all of the AAV-induced cytokines and chemokines can be upregulated by activation of TLR9 in the periphery using synthetic CpG-rich oligonucleotides.8,9,10,11,12,52,53,54,55,56,57,58”
From An innate immune response to adeno-associated virus genomes decreases cortical dendritic complexity and disrupts synaptic transmission (2024) · cites this paper as [56]

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Gorden, K. B., Gorski, K. S., Gibson, S. J., Kedl, R. M., Kieper, W. C., Qiu, X., Tomai, M. A., Alkan, Ş. Ş., & Vasilakos, J. P. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.3.1259 · Cited by 690 · see citing works
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Beignon, A. (2005) · Journal of Clinical Investigation · doi:10.1172/jci26032 · Cited by 674 · see citing works
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Mandl, J. N., Barry, A. P., Vanderford, T. H., Kozyr, N. L., Chavan, R., Klucking, S., Barrat, F. J., Coffman, R. L., Staprans, S. I., & Feinberg, M. B. (2008) · Nature Medicine · doi:10.1038/nm.1871 · Cited by 382 · see citing works
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Carpentier, P. A., Begolka, W. S., Olson, J. K., Elhofy, A., Karpus, W. J., & Miller, S. D. (2004) · Glia · doi:10.1002/glia.20117 · Cited by 359 · see citing works
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Ma, Y., Li, J., Chiu, I., Wang, Y., Sloane, J., Lu, J.-N., Kosaras, B., Sidman, R., Volpe, J., & Vartanian, T. (2006) · Journal of Cell Biology · doi:10.1083/jcb.200606016 · Cited by 284 · see citing works
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Town, T., Bai, F., Wang, T., Kaplan, A. T., Qian, F., Montgomery, R. R., Anderson, J. F., Flavell, R. A., & Fikrig, E. (2009) · Immunity · doi:10.1016/j.immuni.2008.11.012 · Cited by 217 · see citing works
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Iliev, A. I., Stringaris, A. K., Nau, R., & Neumann, H. (2004) · The FASEB Journal · doi:10.1096/fj.03-0670fje · Cited by 192 · see citing works
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Damm, J., Wiegand, F., Harden, L. M., Gerstberger, R., Rummel, C. D., & Roth, J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.013 · Cited by 52 · see citing works
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Lang, R., Li, H., Luo, X., Liu, C., Zhang, Y., Guo, S., Xu, J., Bao, C., Dong, W., & Yu, Y. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1008072 · Cited by 47 · see citing works
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Kato, J., Agalave, N. M., & Svensson, C. I. (2016) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2016.06.039 · Cited by 44 · see citing works
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Mitterreiter, J. G., Ouwendijk, W. J. D., van Velzen, M., van Nierop, G. P., Osterhaus, A. D. M. E., & Verjans, G. M. G. M. (2017) · European Journal of Immunology · doi:10.1002/eji.201746989 · Cited by 44 · see citing works
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Sanders, M. S., van Well, G. T. J., Ouburg, S., Lundberg, P. S., van Furth, A. M., & Morré, S. A. (2011) · Clinical Infectious Diseases · doi:10.1093/cid/ciq155 · Cited by 43 · see citing works
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Madeddu, S., Woods, T. A., Mukherjee, P., Sturdevant, D. E., Butchi, N. B., & Peterson, K. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127336 · Cited by 42 · see citing works
Self-citation
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Li, J., Faber, M., Dietzschold, B., & Hooper, D. C. (2011) · Advances in virus research · doi:10.1016/b978-0-12-387040-7.00007-x · Cited by 42 · see citing works
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Christensen, L. B., Woods, T. A., Carmody, A., Caughey, B. W., & Peterson, K. E. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-70 · Cited by 42 · see citing works
Self-citation
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Self-citation
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Kapil, P., Butchi, N. B., Stohlman, S. A., & Bergmann, C. C. (2012) · Glia · doi:10.1002/glia.22375 · Cited by 41 · see citing works
Self-citation
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Winkler, C. W., Taylor, K., & Peterson, K. E. (2014) · Science Signaling · doi:10.1126/scisignal.2005407 · Cited by 39 · see citing works
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Lobo‐Silva, D., Carriche, G. M., Castro, A. G., Roque, S., & Saraiva, M. (2017) · Glia · doi:10.1002/glia.23172 · Cited by 35 · see citing works
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Ifuku, M., Buonfiglioli, A., Jordan, P., Lehnardt, S., & Kettenmann, H. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.08.003 · Cited by 35 · see citing works
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Nativel, B., Ramin‐Mangata, S., Mevizou, R., Figuester, A., Andries, J., Iwema, T., Ikewaki, N., Gasque, P., & Viranaïcken, W. (2019) · Immunology · doi:10.1111/imm.13100 · Cited by 34 · see citing works
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Aurelian, L., & Balan, I. S. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05220-4 · Cited by 30 · see citing works
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Cukovic, D., Bagla, S., Ukasik, D., Stemmer, P. M., Jena, B. P., Naik, A. R., Sood, S., Asano, E., Luat, A. F., Chugani, D. C., et al. (2021) · Non-Coding RNA · doi:10.3390/ncrna7030040 · Cited by 30 · see citing works
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Kwon, J., Suessmilch, M., McColl, A., Cavanagh, J., & MORRIS, B. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-03216-9 · Cited by 25 · see citing works
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Szabó, A., Gogolák, P., Pázmándi, K., Kis‐Tóth, K., Riedl, K., Wizel, B., Lingnau, K., Bácsi, A., Réthi, B., & Rajnavölgyi, É. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055264 · Cited by 26 · see citing works
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Hayashi, T., Yao, S., Crain, B., Chan, M., Tawatao, R. I., Gray, C. S., Vuong, L., Lao, F. S., Cottam, H. B., Carson, D. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045860 · Cited by 26 · see citing works
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Holley, M. M., Zhang, Y., Lehrmann, E., Wood, W. H., Becker, K. G., & Kielian, T. (2011) · Glia · doi:10.1002/glia.21243 · Cited by 23 · see citing works
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Clark, I. A., & Vissel, B. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.030 · Cited by 23 · see citing works
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Suriano, C. M., Kumar, N., Verpeut, J. L., Ma, J., Jung, C., Dunn, C. E., Carvajal, B. V., Nguyen, A. V., & Boulanger, L. M. (2024) · Molecular Therapy · doi:10.1016/j.ymthe.2024.03.036 · Cited by 21 · see citing works
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Su, F., Bai, F., Zhou, H., & Zhang, Z. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.05.016 · Cited by 19 · see citing works
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Self-citation
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Vijay, G. K. M., Hu, C., Peng, J., García‐Martinez, I., Hoque, R., Verghis, R. M., Ma, Y., Mehal, W. Z., Shawcross, D. L., & Li, W. (2019) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2019.08.002 · Cited by 18 · see citing works
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Tiwari, R. K., Moin, A., Rizvi, S. M. D., Shahid, S. M. A., & Bajpai, P. (2021) · Metabolic Brain Disease · doi:10.1007/s11011-021-00696-6 · Cited by 18 · see citing works
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Zhao, Y., Pu, D., Sun, Y., Chen, J., Luo, C., Wang, M., Zhou, J., Lv, A., Zhu, S., Liao, Z., et al. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.12.030 · Cited by 16 · see citing works
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Ji, Y., Zhou, Y., Pan, J., Li, X., Wang, H., & Wang, Y. (2015) · International Journal of Neuroscience · doi:10.3109/00207454.2015.1010649 · Cited by 15 · see citing works
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Manangeeswaran, M., Lewkowicz, A. P., Israely, T., Ireland, D. D. C., & Verthelyi, D. I. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00237 · Cited by 14 · see citing works
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Lin, C.-C. J., Wu, Y.-J., Heimrich, B., & Schwemmle, M. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1402-5 · Cited by 13 · see citing works
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Govindarajulu, M., Patel, M. Y., Wilder, D. M., Krishnan, J. K. S., LaValle, C. R., Pandya, J. D., Shear, D. A., Hefeneider, S. H., Long, J. B., & Arun, P. (2023) · Neuroscience Letters · doi:10.1016/j.neulet.2023.137364 · Cited by 12 · see citing works
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Damm, J., Wiegand, F., Harden, L. M., Wenisch, S., Gerstberger, R., Rummel, C. D., & Roth, J. (2014) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2014.10.007 · Cited by 11 · see citing works
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Guo, M., Xu, Y., & Zhang, C. (2021) · Handbook of experimental pharmacology · doi:10.1007/164_2021_542 · Cited by 10 · see citing works
Microvesicles in active lupus nephritis show Toll-like receptor 9-dependent co-expression of galectin-3 binding protein and double-stranded DNA
Rasmussen, N., Nielsen, C. T., Nielsen, C. H., & Jacobsen, S. (2020) · Clinical & Experimental Immunology · doi:10.1111/cei.13569 · Cited by 10 · see citing works
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Kubo, Y., Yanagawa, Y., Matsumoto, M., Hiraide, S., Kobayashi, M., & Togashi, H. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.06.017 · Cited by 9 · see citing works
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Ojha, D., Woods, T. A., & Peterson, K. E. (2021) · Viruses · doi:10.3390/v13112317 · Cited by 9 · see citing works
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Delery, E., & MacLean, A. G. (2018) · Viral Immunology · doi:10.1089/vim.2018.0093 · Cited by 7 · see citing works
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Evans, L. H., Boi, S., Malik, F., Wehrly, K., Peterson, K. E., & Chesebro, B. W. (2014) · Journal of Virological Methods · doi:10.1016/j.jviromet.2014.02.006 · Cited by 7 · see citing works
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Kaufman, E. (2014) · doi:10.6083/m4mc8x1v · Cited by 3 · see citing works
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Gu, L., Zhou, J., Tan, J., Su, L., Wei, Q., Jiang, H., Liang, B., & Tang, Q. (2016) · Journal of Molecular Neuroscience · doi:10.1007/s12031-016-0773-0 · Cited by 3 · see citing works
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Gupta, K. H., Giurini, E. F., & Zloza, A. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1308651 · Cited by 2 · see citing works
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Farahtaj, F., Gholami, A., Khosravy, M. S., Gharibzadeh, S., Niknam, H. M., & Ghaemi, A. (2021) · Microbial Pathogenesis · doi:10.1016/j.micpath.2021.104971 · Cited by 1 · see citing works
Prenatal stress alters offspring neurovascular, autonomic, and immune development in animal models of neuropsychiatric and cardiometabolic disorders
Martinez, M., Castellanos, E., Sheng, J. A., Hale, T. M., & Tobet, S. A. (2026) · Journal of Neuroendocrinology · doi:10.1111/jne.70231 · Cited by 1 · see citing works
The Role of Toll-Like Receptors in CNS Rabies Infection
Ghasemi, S., Gholami, A., Jahanbakhsh, F., Fazeli, M., Anvari, S., & Ghaemi, A. (2015) · The Neuroscience Journal of Shefaye Khatam · doi:10.18869/acadpub.shefa.3.4.131 · Cited by 1 · see citing works
Innate Immune Responses in (Myco) Bacterial Meningitis
van Well, G. T. J. (2012) · Pure Amsterdam UMC
Molecular mechanisms involved in the interaction between the immune system and nervous system
Yanagawa, Y., Kubo, Y., Matsumoto, M., & Togashi, H. (2013) · Folia Pharmacologica Japonica · doi:10.1254/fpj.141.27

Different innate immune profiles by astrocytes and microglia following TLR7 and/or TLR9 agonist stimulation (135.12)
Butchi, N. B., Du, M., & karin, P. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.supp.135.12
Self-citation
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Butchi, N. B. (2009) · doi:10.31390/gradschool_dissertations.2081
Self-citation
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Butchi, N. B., Pourciau, S. S., Du, M., Morgan, T. W., & Peterson, K. E. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.11.7604 · Cited by 82 · see citing works
Self-citation
Unique gene expression profiles of microglia and astrocytes following innate immune activation
Madeddu, S. (2014) · VEprints - Universita degli Studi di Cagliari
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Butchi, N. B., Woods, T. A., Du, M., Morgan, T. W., & Peterson, K. E. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.04.011 · Cited by 59 · see citing works
Self-citation

Authors: Butchi, N. B., Du, M., & Peterson, K. E.
Affiliations: National Institute of Allergy and Infectious Diseases (US)
Corresponding author: Peterson, Karin E.
ORCID: Peterson, Karin E.
Venue: Glia
Publisher: Wiley
Published: 2009-12-08
Volume: 58
Issue: 6
Pages: 650-664
ISSN: 0894-1491 (ISSN-L)
1098-1136
DOI: 10.1002/glia.20952
PMC: PMC3767435
OpenAlex: W1970216950
Cited by: 109
References: 41
Citations by year: 2026: 7 · 2025: 5 · 2024: 4 · 2023: 2 · 2022: 4 · 2021: 10 · 2020: 5 · 2019: 7 · 2018: 4 · 2017: 4 · 2016: 8 · 2015: 7 · 2014: 11 · 2013: 8 · 2012: 8
FWCI: 3.16
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Glia (publishedVersion, public-domain)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
Centers for Disease Control and Prevention (IP20RR020159)
National Institute of Allergy and Infectious Diseases (ZIAAI001101)
National Center for Research Resources (P20RR020159)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Keywords: TLR7, TLR9, TLR agonists, imiquimod, CpG oligodeoxynucleotides, astrocytes, microglia, innate immune response, cytokine profile, IL-10, granulocyte colony-stimulating factor, IL-9, MyD88 signaling, costimulation
MeSH terms: Imiquimod, Adjuvants, Immunologic, Aminoquinolines, Analysis of Variance, Animals, Astrocytes, Cells, Cultured, Cerebral Cortex, Dose-Response Relationship, Drug, Embryo, Mammalian, Flow Cytometry, Gene Expression Regulation, Membrane Glycoproteins, Mice, Inbred C57BL, Nerve Tissue Proteins, Neurons, Oligodeoxyribonucleotides, RNA, Messenger, Signal Transduction, Cytokines, Apoptosis, Microglia, Mice, Knockout, Toll-Like Receptor 7, Toll-Like Receptor 9, Mice

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Interactions between TLR7 and TLR9 agonists and receptors regulate innate immune responses by astrocytes and microglia

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