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Unlike similar viruses such as SARS-CoV-2, EEEV replicates efficiently in neurons, producing progeny viral particles as soon as 3\u20134 hours post-infection. EEEV infection, which can cause severe encephalitis with a human mortality rate surpassing 30%, has no licensed, targeted therapies, leaving patients to rely on supportive care. Although the general characteristics of EEEV infection within the host cell are well-studied, it remains unclear how these interactions lead to rapid production of progeny viral particles, limiting development of antiviral therapies. Here, we present a novel rule-based model that describes attachment, entry, uncoating, replication, assembly, and export of both infectious virions and virus-like particles within mammalian cells. Additionally, it quantitatively characterizes host ribosome activity in EEEV replication via a model parameter defining ribosome density on viral RNA. To calibrate the model, we performed experiments to quantify viral RNA, protein, and infectious particle production during acute infection. We used Bayesian inference to calibrate the model, discovering in the process that an additional constraint was required to ensure consistency with previous experimental observations of a high ratio between the amounts of full-length positive-sense viral genome and negative-sense template strand. Overall, the model recapitulates the experimental data and predicts that EEEV rapidly concentrates host ribosomes densely on viral RNA. Dense packing of host ribosomes was determined to be critical to establishing the characteristic positive to negative RNA strand ratio because of its role in governing the kinetics of transcription. Sensitivity analysis identified viral transcription as the critical step for infectious particle production, making it a potential target for future therapeutic development.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1013082","type":"journal-article","created":{"date-parts":[[2025,6,4]],"date-time":"2025-06-04T13:29:27Z","timestamp":1749043767000},"page":"e1013082","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["A detailed kinetic model of Eastern equine encephalitis virus replication in a susceptible host cell"],"prefix":"10.1371","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0206-277X","authenticated-orcid":true,"given":"Caroline I.","family":"Larkin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew D.","family":"Dunn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3315-7103","authenticated-orcid":true,"given":"Jason E.","family":"Shoemaker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4506-7842","authenticated-orcid":true,"given":"William B.","family":"Klimstra","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8127-609X","authenticated-orcid":true,"given":"James R.","family":"Faeder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,6,4]]},"reference":[{"issue":"5","key":"pcbi.1013082.ref001","doi-asserted-by":"crossref","first-page":"1472","DOI":"10.4269\/ajtmh.17-0927","article-title":"Eastern equine encephalitis virus in the United States, 2003\u20132016","volume":"98","author":"NP Lindsey","year":"2018","journal-title":"Am J Trop Med Hyg"},{"issue":"26","key":"pcbi.1013082.ref002","doi-asserted-by":"crossref","first-page":"1867","DOI":"10.1056\/NEJM199706263362604","article-title":"Clinical and neuroradiographic manifestations of eastern equine encephalitis","volume":"336","author":"RL Deresiewicz","year":"1997","journal-title":"N Engl J Med"},{"key":"pcbi.1013082.ref003","doi-asserted-by":"crossref","first-page":"959","DOI":"10.3389\/fmicb.2016.00959","article-title":"Neurological sequelae resulting from encephalitic alphavirus infection","volume":"7","author":"SE Ronca","year":"2016","journal-title":"Front Microbiol"},{"issue":"3","key":"pcbi.1013082.ref004","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1086\/519391","article-title":"Severe encephalitis in cynomolgus macaques exposed to aerosolized Eastern equine encephalitis virus","volume":"196","author":"DS Reed","year":"2007","journal-title":"J Infect Dis"},{"issue":"1","key":"pcbi.1013082.ref005","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1186\/s12985-017-0687-7","article-title":"Characterization and pathogenesis of aerosolized eastern equine encephalitis in the common marmoset (Callithrix jacchus)","volume":"14","author":"AI Porter","year":"2017","journal-title":"Virol J"},{"issue":"1","key":"pcbi.1013082.ref006","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/s12985-018-1103-7","article-title":"Aerosol infection of Balb\/c mice with eastern equine encephalitis virus; susceptibility and lethality","volume":"16","author":"AL Phelps","year":"2019","journal-title":"Virol J"},{"issue":"2","key":"pcbi.1013082.ref007","article-title":"Physiological and immunological changes in the brain associated with lethal eastern equine encephalitis virus in macaques","volume":"17","author":"JR Albe","year":"2021","journal-title":"PLoS Pathog"},{"issue":"21","key":"pcbi.1013082.ref008","doi-asserted-by":"crossref","first-page":"1989","DOI":"10.1056\/NEJMp1914328","article-title":"Eastern equine encephalitis virus - another emergent arbovirus in the United States","volume":"381","author":"DM Morens","year":"2019","journal-title":"N Engl J Med"},{"key":"pcbi.1013082.ref009","unstructured":"Centers for Disease Control and Prevention. 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