{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T06:24:41Z","timestamp":1790835881624,"version":"4.1.0"},"reference-count":66,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,4,24]],"date-time":"2024-04-24T00:00:00Z","timestamp":1713916800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,4,24]],"date-time":"2024-04-24T00:00:00Z","timestamp":1713916800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100006492","name":"Division of Intramural Research, National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100006492","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Commun Biol"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Inflammatory monocytes (iMO) are recruited from the bone marrow to the brain during viral encephalitis. C-C motif chemokine receptor (CCR) 2 deficiency substantially reduces iMO recruitment for most, but not all encephalitic viruses. Here we show CCR7 acts synergistically with CCR2 to control this process. Following Herpes simplex virus type-1 (HSV-1), or La Crosse virus (LACV) infection, we find iMO proportions are reduced by approximately half in either <jats:italic>Ccr2<\/jats:italic> or <jats:italic>Ccr7<\/jats:italic> knockout mice compared to control mice. However, <jats:italic>Ccr2<\/jats:italic>\/<jats:italic>Ccr7<\/jats:italic> double knockouts eliminate iMO recruitment following infection with either virus, indicating these receptors together control iMO recruitment. We also find that LACV induces a more robust iMO recruitment than HSV-1. However, unlike iMOs in HSV-1 infection, LACV-recruited iMOs do not influence neurological disease development. LACV-induced iMOs have higher expression of proinflammatory and proapoptotic but reduced mitotic, phagocytic and phagolysosomal transcripts compared to HSV-1-induced iMOs. Thus, virus-specific activation of iMOs affects their recruitment, activation, and function.<\/jats:p>","DOI":"10.1038\/s42003-024-06178-6","type":"journal-article","created":{"date-parts":[[2024,4,24]],"date-time":"2024-04-24T10:01:49Z","timestamp":1713952909000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["C-C motif chemokine receptor 2 and 7 synergistically control inflammatory monocyte recruitment but the infecting virus dictates monocyte function in the brain"],"prefix":"10.1038","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4460-3378","authenticated-orcid":false,"given":"Clayton W.","family":"Winkler","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3766-9272","authenticated-orcid":false,"given":"Alyssa B.","family":"Evans","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aaron B.","family":"Carmody","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Justin B.","family":"Lack","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tyson A.","family":"Woods","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karin E.","family":"Peterson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,4,24]]},"reference":[{"key":"6178_CR1","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1056\/NEJM200103153441103","volume":"344","author":"JE McJunkin","year":"2001","unstructured":"McJunkin, J. E. et al. La Crosse encephalitis in children. N. Engl. J. Med. 344, 801\u2013807 (2001).","journal-title":"N. Engl. J. Med."},{"key":"6178_CR2","unstructured":"Centers for Disease Control and Prevention. La Crosse Encephalitis Virus (Centers for Disease Control and Prevention; 2022)."},{"key":"6178_CR3","doi-asserted-by":"crossref","unstructured":"Boutzoukas A. E., et al. La Crosse Virus Neuroinvasive Disease in Children: A Contemporary Analysis of Clinical\/Neurobehavioral Outcomes and Predictors of Disease Severity. Clin. Infect. Dis. 76, e1114\u2013e1122 (2023).","DOI":"10.1093\/cid\/ciac403"},{"key":"6178_CR4","doi-asserted-by":"publisher","first-page":"11070","DOI":"10.1128\/JVI.01866-14","volume":"88","author":"KG Taylor","year":"2014","unstructured":"Taylor, K. G., Woods, T. A., Winkler, C. W., Carmody, A. B. & Peterson, K. E. Age-dependent myeloid dendritic cell responses mediate resistance to la crosse virus-induced neurological disease. J. Virol. 88, 11070\u201311079 (2014).","journal-title":"J. Virol."},{"key":"6178_CR5","doi-asserted-by":"publisher","DOI":"10.1186\/s12974-017-0836-3","volume":"14","author":"CW Winkler","year":"2017","unstructured":"Winkler, C. W. et al. Lymphocytes have a role in protection, but not in pathogenesis, during La Crosse Virus infection in mice. J. Neuroinflammation 14, 62 (2017).","journal-title":"J. Neuroinflammation"},{"key":"6178_CR6","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1186\/1743-422X-5-25","volume":"5","author":"RS Bennett","year":"2008","unstructured":"Bennett, R. S. et al. La Crosse virus infectivity, pathogenesis, and immunogenicity in mice and monkeys. Virol. J. 5, 25 (2008).","journal-title":"Virol. J."},{"key":"6178_CR7","doi-asserted-by":"publisher","first-page":"471","DOI":"10.4049\/jimmunol.1701230","volume":"200","author":"CW Winkler","year":"2018","unstructured":"Winkler, C. W. et al. Cutting Edge: CCR2 Is Not Required for Ly6C(hi) Monocyte Egress from the Bone Marrow but Is Necessary for Migration within the Brain in La Crosse Virus Encephalitis. J. Immunol. 200, 471\u2013476 (2018).","journal-title":"J. Immunol."},{"key":"6178_CR8","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1161\/ATVBAHA.116.308198","volume":"37","author":"RM Kratofil","year":"2017","unstructured":"Kratofil, R. M., Kubes, P. & Deniset, J. F. Monocyte Conversion During Inflammation and Injury. Arterioscler. Thromb. Vasc. Biol. 37, 35\u201342 (2017).","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"6178_CR9","doi-asserted-by":"publisher","DOI":"10.1186\/1742-2094-9-270","volume":"9","author":"RL Terry","year":"2012","unstructured":"Terry, R. L. et al. Inflammatory monocytes and the pathogenesis of viral encephalitis. J. Neuroinflammation 9, 270 (2012).","journal-title":"J. Neuroinflammation"},{"key":"6178_CR10","doi-asserted-by":"publisher","DOI":"10.1186\/2050-7771-2-1","volume":"2","author":"J Yang","year":"2014","unstructured":"Yang, J., Zhang, L., Yu, C., Yang, X. F. & Wang, H. Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark. Res. 2, 1 (2014).","journal-title":"Biomark. Res."},{"key":"6178_CR11","doi-asserted-by":"publisher","first-page":"1294","DOI":"10.1099\/vir.0.041046-0","volume":"93","author":"N Boivin","year":"2012","unstructured":"Boivin, N., Menasria, R., Gosselin, D., Rivest, S. & Boivin, G. Impact of deficiency in CCR2 and CX3CR1 receptors on monocytes trafficking in herpes simplex virus encephalitis. J. Gen. Virol. 93, 1294\u20131304 (2012).","journal-title":"J. Gen. Virol."},{"key":"6178_CR12","doi-asserted-by":"publisher","first-page":"e0168034","DOI":"10.1371\/journal.pone.0168034","volume":"11","author":"R Menasria","year":"2016","unstructured":"Menasria, R., Canivet, C., Piret, J., Gosselin, J. & Boivin, G. Both Cerebral and Hematopoietic Deficiencies in CCR2 Result in Uncontrolled Herpes Simplex Virus Infection of the Central Nervous System in Mice. PLoS One 11, e0168034 (2016).","journal-title":"PLoS One"},{"key":"6178_CR13","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2020.108150","volume":"32","author":"BD Michael","year":"2020","unstructured":"Michael, B. D. et al. Astrocyte- and Neuron-Derived CXCL1 Drives Neutrophil Transmigration and Blood-Brain Barrier Permeability in Viral Encephalitis. Cell Rep. 32, 108150 (2020).","journal-title":"Cell Rep."},{"key":"6178_CR14","doi-asserted-by":"publisher","first-page":"471","DOI":"10.4049\/jimmunol.1003003","volume":"186","author":"JK Lim","year":"2011","unstructured":"Lim, J. K. et al. Chemokine receptor Ccr2 is critical for monocyte accumulation and survival in West Nile virus encephalitis. J. Immunol. 186, 471\u2013478 (2011).","journal-title":"J. Immunol."},{"key":"6178_CR15","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1038\/nature07591","volume":"457","author":"JV Kim","year":"2009","unstructured":"Kim, J. V., Kang, S. S., Dustin, M. L. & McGavern, D. B. Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature 457, 191\u2013195 (2009).","journal-title":"Nature"},{"key":"6178_CR16","doi-asserted-by":"publisher","first-page":"219ra217","DOI":"10.1126\/scitranslmed.3007563","volume":"6","author":"DR Getts","year":"2014","unstructured":"Getts, D. R. et al. Therapeutic inflammatory monocyte modulation using immune-modifying microparticles. Sci. Transl. Med. 6, 219ra217 (2014).","journal-title":"Sci. Transl. Med."},{"key":"6178_CR17","doi-asserted-by":"publisher","first-page":"902","DOI":"10.1172\/JCI29919","volume":"117","author":"CL Tsou","year":"2007","unstructured":"Tsou, C. L. et al. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J. Clin. Invest. 117, 902\u2013909 (2007).","journal-title":"J. Clin. Invest."},{"key":"6178_CR18","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1038\/mi.2012.46","volume":"6","author":"CD Conrady","year":"2013","unstructured":"Conrady, C. D., Zheng, M., Mandal, N. A., van Rooijen, N. & Carr, D. J. IFN-alpha-driven CCL2 production recruits inflammatory monocytes to infection site in mice. Mucosal. Immunol. 6, 45\u201355 (2013).","journal-title":"Mucosal. Immunol."},{"key":"6178_CR19","doi-asserted-by":"publisher","first-page":"8050","DOI":"10.1128\/JVI.76.16.8050-8057.2002","volume":"76","author":"TM Tumpey","year":"2002","unstructured":"Tumpey, T. M., Fenton, R., Molesworth-Kenyon, S., Oakes, J. E. & Lausch, R. N. Role for macrophage inflammatory protein 2 (MIP-2), MIP-1alpha, and interleukin-1alpha in the delayed-type hypersensitivity response to viral antigen. J. Virol. 76, 8050\u20138057 (2002).","journal-title":"J. Virol."},{"key":"6178_CR20","doi-asserted-by":"publisher","DOI":"10.1186\/s12974-017-1015-2","volume":"14","author":"CL Howe","year":"2017","unstructured":"Howe, C. L., LaFrance-Corey, R. G., Goddery, E. N., Johnson, R. K. & Mirchia, K. Neuronal CCL2 expression drives inflammatory monocyte infiltration into the brain during acute virus infection. J. Neuroinflammation 14, 238 (2017).","journal-title":"J. Neuroinflammation"},{"key":"6178_CR21","doi-asserted-by":"publisher","first-page":"1719","DOI":"10.1002\/glia.23642","volume":"67","author":"PL Bozzelli","year":"2019","unstructured":"Bozzelli, P. L. et al. HIV-1 Tat promotes astrocytic release of CCL2 through MMP\/PAR-1 signaling. Glia 67, 1719\u20131729 (2019).","journal-title":"Glia"},{"key":"6178_CR22","doi-asserted-by":"publisher","first-page":"e0128387","DOI":"10.1371\/journal.pone.0128387","volume":"10","author":"H Jung","year":"2015","unstructured":"Jung, H., Mithal, D. S., Park, J. E. & Miller, R. J. Localized CCR2 Activation in the Bone Marrow Niche Mobilizes Monocytes by Desensitizing CXCR4. PLoS One 10, e0128387 (2015).","journal-title":"PLoS One"},{"key":"6178_CR23","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1016\/j.immuni.2011.04.008","volume":"34","author":"Y Zhu","year":"2011","unstructured":"Zhu, Y., Yao, S. & Chen, L. Cell surface signaling molecules in the control of immune responses: a tide model. Immunity 34, 466\u2013478 (2011).","journal-title":"Immunity"},{"key":"6178_CR24","doi-asserted-by":"publisher","first-page":"4580","DOI":"10.1128\/JVI.76.9.4580-4590.2002","volume":"76","author":"AK Zaiss","year":"2002","unstructured":"Zaiss, A. K. et al. Differential activation of innate immune responses by adenovirus and adeno-associated virus vectors. J. Virol. 76, 4580\u20134590 (2002).","journal-title":"J. Virol."},{"key":"6178_CR25","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2020.575074","volume":"11","author":"W Bouwman","year":"2020","unstructured":"Bouwman, W., Verhaegh, W., Holtzer, L. & van de Stolpe, A. Measurement of Cellular Immune Response to Viral Infection and Vaccination. Front. Immunol. 11, 575074 (2020).","journal-title":"Front. Immunol."},{"key":"6178_CR26","doi-asserted-by":"publisher","first-page":"1231","DOI":"10.1084\/jem.20032152","volume":"200","author":"C Qu","year":"2004","unstructured":"Qu, C. et al. Role of CCR8 and other chemokine pathways in the migration of monocyte-derived dendritic cells to lymph nodes. J. Exp. Med. 200, 1231\u20131241 (2004).","journal-title":"J. Exp. Med."},{"key":"6178_CR27","doi-asserted-by":"publisher","first-page":"1287","DOI":"10.4049\/jimmunol.182.3.1287","volume":"182","author":"Z Bai","year":"2009","unstructured":"Bai, Z. et al. CXC chemokine ligand 12 promotes CCR7-dependent naive T cell trafficking to lymph nodes and Peyer\u2019s patches. J. Immunol. 182, 1287\u20131295 (2009).","journal-title":"J. Immunol."},{"key":"6178_CR28","doi-asserted-by":"publisher","first-page":"53","DOI":"10.4049\/jimmunol.1002358","volume":"186","author":"BG Ricart","year":"2011","unstructured":"Ricart, B. G., John, B., Lee, D., Hunter, C. A. & Hammer, D. A. Dendritic cells distinguish individual chemokine signals through CCR7 and CXCR4. J. Immunol. 186, 53\u201361 (2011).","journal-title":"J. Immunol."},{"key":"6178_CR29","doi-asserted-by":"publisher","first-page":"3578","DOI":"10.4049\/jimmunol.176.6.3578","volume":"176","author":"C Jakubzick","year":"2006","unstructured":"Jakubzick, C., Tacke, F., Llodra, J., van Rooijen, N. & Randolph, G. J. Modulation of dendritic cell trafficking to and from the airways. J. Immunol. 176, 3578\u20133584 (2006).","journal-title":"J. Immunol."},{"key":"6178_CR30","doi-asserted-by":"publisher","first-page":"e79098","DOI":"10.1371\/journal.pone.0079098","volume":"8","author":"JC Kling","year":"2013","unstructured":"Kling, J. C., Mack, M. & Korner, H. The absence of CCR7 results in dysregulated monocyte migration and immunosuppression facilitating chronic cutaneous leishmaniasis. PLoS One 8, e79098 (2013).","journal-title":"PLoS One"},{"key":"6178_CR31","doi-asserted-by":"publisher","first-page":"6846","DOI":"10.4049\/jimmunol.180.10.6846","volume":"180","author":"T Jia","year":"2008","unstructured":"Jia, T. et al. Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J. Immunol. 180, 6846\u20136853 (2008).","journal-title":"J. Immunol."},{"key":"6178_CR32","doi-asserted-by":"publisher","first-page":"e13693","DOI":"10.1371\/journal.pone.0013693","volume":"5","author":"N Saederup","year":"2010","unstructured":"Saederup, N. et al. Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS One 5, e13693 (2010).","journal-title":"PLoS One"},{"key":"6178_CR33","doi-asserted-by":"publisher","first-page":"532","DOI":"10.1093\/jleuko\/qiad093","volume":"114","author":"J Pang","year":"2023","unstructured":"Pang, J. & Koh, T. J. Proliferation of monocytes and macrophages in homeostasis, infection, injury, and disease. J. Leukoc. Biol. 114, 532\u2013546 (2023).","journal-title":"J. Leukoc. Biol."},{"key":"6178_CR34","doi-asserted-by":"publisher","DOI":"10.1016\/j.smim.2019.05.001","volume":"43","author":"S Lukhele","year":"2019","unstructured":"Lukhele, S., Boukhaled, G. M. & Brooks, D. G. Type I interferon signaling, regulation and gene stimulation in chronic virus infection. Semin. Immunol. 43, 101277 (2019).","journal-title":"Semin. Immunol."},{"key":"6178_CR35","doi-asserted-by":"publisher","first-page":"8057","DOI":"10.3390\/ijms21218057","volume":"21","author":"J Arnhold","year":"2020","unstructured":"Arnhold, J. The Dual Role of Myeloperoxidase in Immune Response. Int J. Mol. Sci. 21, 8057 (2020).","journal-title":"Int J. Mol. Sci."},{"key":"6178_CR36","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1016\/j.it.2017.03.006","volume":"38","author":"AM Pauwels","year":"2017","unstructured":"Pauwels, A. M., Trost, M., Beyaert, R. & Hoffmann, E. Patterns, Receptors, and Signals: Regulation of Phagosome Maturation. Trends Immunol. 38, 407\u2013422 (2017).","journal-title":"Trends Immunol."},{"key":"6178_CR37","doi-asserted-by":"crossref","unstructured":"Jaumouille, V. & Grinstein, S. Molecular Mechanisms of Phagosome Formation. Microbiol. Spectr. 4, 1\u201318 (2016).","DOI":"10.1128\/microbiolspec.MCHD-0013-2015"},{"key":"6178_CR38","doi-asserted-by":"publisher","first-page":"4195","DOI":"10.1111\/bph.14470","volume":"175","author":"BJ Gu","year":"2018","unstructured":"Gu, B. J. & Wiley, J. S. P2X7 as a scavenger receptor for innate phagocytosis in the brain. Br. J. Pharm. 175, 4195\u20134208 (2018).","journal-title":"Br. J. Pharm."},{"key":"6178_CR39","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1080\/15548627.2018.1434374","volume":"14","author":"Y Song","year":"2018","unstructured":"Song, Y., Shang, D., Cheng, H. & Zhou, R. The small GTPase RAB37 functions as an organizer for autophagosome biogenesis. Autophagy 14, 727\u2013729 (2018).","journal-title":"Autophagy"},{"key":"6178_CR40","doi-asserted-by":"publisher","first-page":"1066","DOI":"10.3389\/fimmu.2020.01066","volume":"11","author":"E Uribe-Querol","year":"2020","unstructured":"Uribe-Querol, E. & Rosales, C. Phagocytosis: Our Current Understanding of a Universal Biological Process. Front. Immunol. 11, 1066 (2020).","journal-title":"Front. Immunol."},{"key":"6178_CR41","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1111\/tra.12199","volume":"15","author":"GH Kim","year":"2014","unstructured":"Kim, G. H., Dayam, R. M., Prashar, A., Terebiznik, M. & Botelho, R. J. PIKfyve inhibition interferes with phagosome and endosome maturation in macrophages. Traffic 15, 1143\u20131163 (2014).","journal-title":"Traffic"},{"key":"6178_CR42","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.636078","volume":"12","author":"JA Nguyen","year":"2021","unstructured":"Nguyen, J. A. & Yates, R. M. Better Together: Current Insights Into Phagosome-Lysosome Fusion. Front. Immunol. 12, 636078 (2021).","journal-title":"Front. Immunol."},{"key":"6178_CR43","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1038\/ni1309","volume":"7","author":"NV Serbina","year":"2006","unstructured":"Serbina, N. V. & Pamer, E. G. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311\u2013317 (2006).","journal-title":"Nat. Immunol."},{"key":"6178_CR44","doi-asserted-by":"publisher","first-page":"378","DOI":"10.1016\/j.immuni.2019.01.009","volume":"50","author":"DP Dyer","year":"2019","unstructured":"Dyer, D. P. et al. Chemokine Receptor Redundancy and Specificity Are Context Dependent. Immunity 50, 378\u2013389 e375 (2019).","journal-title":"Immunity"},{"key":"6178_CR45","doi-asserted-by":"publisher","DOI":"10.1038\/srep11664","volume":"5","author":"N Fujimura","year":"2015","unstructured":"Fujimura, N. et al. CCR2 inhibition sequesters multiple subsets of leukocytes in the bone marrow. Sci. Rep. 5, 11664 (2015).","journal-title":"Sci. Rep."},{"key":"6178_CR46","doi-asserted-by":"publisher","first-page":"4","DOI":"10.2174\/1566524017666170220102732","volume":"17","author":"L Liu","year":"2017","unstructured":"Liu, L., Wei, Y. & Wei, X. The Immune Function of Ly6Chi Inflammatory Monocytes During Infection and Inflammation. Curr. Mol. Med. 17, 4\u201312 (2017).","journal-title":"Curr. Mol. Med."},{"key":"6178_CR47","doi-asserted-by":"publisher","first-page":"1076","DOI":"10.1016\/j.immuni.2012.08.026","volume":"37","author":"E Zigmond","year":"2012","unstructured":"Zigmond, E. et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37, 1076\u20131090 (2012).","journal-title":"Immunity"},{"key":"6178_CR48","doi-asserted-by":"publisher","first-page":"e1002105","DOI":"10.1371\/journal.ppat.1002105","volume":"7","author":"C Le Nouen","year":"2011","unstructured":"Le Nouen, C. et al. Low CCR7-mediated migration of human monocyte derived dendritic cells in response to human respiratory syncytial virus and human metapneumovirus. PLoS Pathog. 7, e1002105 (2011).","journal-title":"PLoS Pathog."},{"key":"6178_CR49","doi-asserted-by":"publisher","first-page":"2779","DOI":"10.3389\/fimmu.2019.02779","volume":"10","author":"KL Monaghan","year":"2019","unstructured":"Monaghan, K. L., Zheng, W., Hu, G. & Wan, E. C. K. Monocytes and Monocyte-Derived Antigen-Presenting Cells Have Distinct Gene Signatures in Experimental Model of Multiple Sclerosis. Front. Immunol. 10, 2779 (2019).","journal-title":"Front. Immunol."},{"key":"6178_CR50","first-page":"918016","volume":"2013","author":"MA Allaire","year":"2013","unstructured":"Allaire, M. A., Tanne, B., Cote, S. C. & Dumais, N. Prostaglandin E 2 Does Not Modulate CCR7 Expression and Functionality after Differentiation of Blood Monocytes into Macrophages. Int. J. Inflam. 2013, 918016 (2013).","journal-title":"Int. J. Inflam."},{"key":"6178_CR51","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1016\/j.immuni.2011.05.009","volume":"34","author":"S Nish","year":"2011","unstructured":"Nish, S. & Medzhitov, R. Host defense pathways: role of redundancy and compensation in infectious disease phenotypes. Immunity 34, 629\u2013636 (2011).","journal-title":"Immunity"},{"key":"6178_CR52","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1111\/imr.12752","volume":"289","author":"T Lammermann","year":"2019","unstructured":"Lammermann, T. & Kastenmuller, W. Concepts of GPCR-controlled navigation in the immune system. Immunol. Rev. 289, 205\u2013231 (2019).","journal-title":"Immunol. Rev."},{"key":"6178_CR53","doi-asserted-by":"publisher","first-page":"705","DOI":"10.1016\/j.immuni.2013.02.013","volume":"38","author":"P Mukherjee","year":"2013","unstructured":"Mukherjee, P., Woods, T. A., Moore, R. A. & Peterson, K. E. Activation of the innate signaling molecule MAVS by bunyavirus infection upregulates the adaptor protein SARM1, leading to neuronal death. Immunity 38, 705\u2013716 (2013).","journal-title":"Immunity"},{"key":"6178_CR54","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1007\/s00401-015-1433-0","volume":"130","author":"CW Winkler","year":"2015","unstructured":"Winkler, C. W., Race, B., Phillips, K. & Peterson, K. E. Capillaries in the olfactory bulb but not the cortex are highly susceptible to virus-induced vascular leak and promote viral neuroinvasion. Acta Neuropathol. 130, 233\u2013245 (2015).","journal-title":"Acta Neuropathol."},{"key":"6178_CR55","doi-asserted-by":"publisher","first-page":"728","DOI":"10.3201\/eid2504.181016","volume":"25","author":"AB Evans","year":"2019","unstructured":"Evans, A. B., Winkler, C. W. & Peterson, K. E. Differences in Neuropathogenesis of Encephalitic California Serogroup Viruses. Emerg. Infect. Dis. 25, 728\u2013738 (2019).","journal-title":"Emerg. Infect. Dis."},{"key":"6178_CR56","doi-asserted-by":"publisher","first-page":"10086","DOI":"10.1128\/JVI.78.18.10086-10095.2004","volume":"78","author":"WP Halford","year":"2004","unstructured":"Halford, W. P., Balliet, J. W. & Gebhardt, B. M. Re-evaluating natural resistance to herpes simplex virus type 1. J. Virol. 78, 10086\u201310095 (2004).","journal-title":"J. Virol."},{"key":"6178_CR57","doi-asserted-by":"publisher","first-page":"2552","DOI":"10.1172\/JCI119798","volume":"100","author":"L Boring","year":"1997","unstructured":"Boring, L. et al. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100, 2552\u20132561 (1997).","journal-title":"J. Clin. Invest."},{"key":"6178_CR58","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/S0092-8674(00)80059-8","volume":"99","author":"R Forster","year":"1999","unstructured":"Forster, R. et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99, 23\u201333 (1999).","journal-title":"Cell"},{"key":"6178_CR59","doi-asserted-by":"publisher","first-page":"143","DOI":"10.4049\/jimmunol.1901289","volume":"205","author":"CW Winkler","year":"2020","unstructured":"Winkler, C. W., Evans, A. B., Carmody, A. B. & Peterson, K. E. Placental Myeloid Cells Protect against Zika Virus Vertical Transmission in a Rag1-Deficient Mouse Model. J. Immunol. 205, 143\u2013152 (2020).","journal-title":"J. Immunol."},{"key":"6178_CR60","doi-asserted-by":"publisher","first-page":"e1010384","DOI":"10.1371\/journal.ppat.1010384","volume":"18","author":"AB Evans","year":"2022","unstructured":"Evans, A. B., Winkler, C. W. & Peterson, K. E. Differences in neuroinvasion and protective innate immune pathways between encephalitic California Serogroup orthobunyaviruses. PLoS Pathog. 18, e1010384 (2022).","journal-title":"PLoS Pathog."},{"key":"6178_CR61","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1016\/j.ajpath.2011.04.011","volume":"179","author":"NB Butchi","year":"2011","unstructured":"Butchi, N. B., Woods, T., Du, M., Morgan, T. W. & Peterson, K. E. TLR7 and TLR9 trigger distinct neuroinflammatory responses in the CNS. Am. J. Pathol. 179, 783\u2013794 (2011).","journal-title":"Am. J. Pathol."},{"key":"6178_CR62","doi-asserted-by":"crossref","unstructured":"Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMDnetjournal. 17, 1\u20133 (2011).","DOI":"10.14806\/ej.17.1.200"},{"key":"6178_CR63","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","volume":"29","author":"A Dobin","year":"2013","unstructured":"Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15\u201321 (2013).","journal-title":"Bioinformatics"},{"key":"6178_CR64","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-12-323","volume":"12","author":"B Li","year":"2011","unstructured":"Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma. 12, 323 (2011).","journal-title":"BMC Bioinforma."},{"key":"6178_CR65","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).","journal-title":"Genome Biol."},{"key":"6178_CR66","doi-asserted-by":"publisher","first-page":"W566","DOI":"10.1093\/nar\/gkv468","volume":"43","author":"T Metsalu","year":"2015","unstructured":"Metsalu, T. & Vilo, J. ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 43, W566\u2013W570 (2015).","journal-title":"Nucleic Acids Res."}],"container-title":["Communications Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s42003-024-06178-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-024-06178-6","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-024-06178-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,24]],"date-time":"2024-04-24T11:20:03Z","timestamp":1713957603000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s42003-024-06178-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,24]]},"references-count":66,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["6178"],"URL":"https:\/\/doi.org\/10.1038\/s42003-024-06178-6","relation":{},"ISSN":["2399-3642"],"issn-type":[{"value":"2399-3642","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,24]]},"assertion":[{"value":"29 March 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 April 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 April 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"494"}}