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Peripheral immune responses to filoviruses in a reservoir versus spillover hosts reveal transcriptional correlates of disease.

ABSTRACT: Several filoviruses, including Marburg virus (MARV), cause severe disease in humans and nonhuman primates (NHPs). However, the Egyptian rousette bat (ERB, Rousettus aegyptiacus), the only known MARV reservoir, shows no overt illness upon natural or experimental infection, which, like other bat hosts of zoonoses, is due to well-adapted, likely species-specific immune features. Despite advances in understanding reservoir immune responses to filoviruses, ERB peripheral blood responses to MARV and how they compare to those of diseased filovirus-infected spillover hosts remain ill-defined. We thus conducted a longitudinal analysis of ERB blood gene responses during acute MARV infection. These data were then contrasted with a compilation of published primate blood response studies to elucidate gene correlates of filovirus protection versus disease. Our work expands on previous findings in MARV-infected ERBs by supporting both host resistance and disease tolerance mechanisms, offers insight into the peripheral immunocellular repertoire during infection, and provides the most direct known cross-examination between reservoir and spillover hosts of the most prevalently-regulated response genes, pathways and activities associated with differences in filovirus pathogenesis and pathogenicity.

SUBMITTER: Guito JC

PROVIDER: S-EPMC10800976 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Peripheral immune responses to filoviruses in a reservoir versus spillover hosts reveal transcriptional correlates of disease.

Guito Jonathan C JC Arnold Catherine E CE Schuh Amy J AJ Amman Brian R BR Sealy Tara K TK Spengler Jessica R JR Harmon Jessica R JR Coleman-McCray Joann D JD Sanchez-Lockhart Mariano M Palacios Gustavo F GF Towner Jonathan S JS Prescott Joseph B JB

Frontiers in immunology 20240108

Several filoviruses, including Marburg virus (MARV), cause severe disease in humans and nonhuman primates (NHPs). However, the Egyptian rousette bat (ERB, <i>Rousettus aegyptiacus</i>), the only known MARV reservoir, shows no overt illness upon natural or experimental infection, which, like other bat hosts of zoonoses, is due to well-adapted, likely species-specific immune features. Despite advances in understanding reservoir immune responses to filoviruses, ERB peripheral blood responses to MAR ...[more]

PMID: 38259437

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Project description:Orthohantaviruses (genus Orthohantavirus) are a diverse group of viruses that are closely associated with their natural hosts (rodents, shrews, and moles). Several orthohantaviruses cause severe disease in humans. Central and western Europe are areas with emerging orthohantavirus occurrences. In our study, several orthohantaviruses, including the pathogenic Kurkino virus (KURV), were detected in their natural hosts trapped at several study sites in the Czech Republic. KURV was detected mainly in its typical host, the striped field mouse (Apodemus agrarius). Nevertheless, spillover infections were also detected in wood mice (Apodemus sylvaticus) and common voles (Microtus arvalis). Similarly, Tula virus (TULV) was found primarily in common voles, and events of spillover to rodents of other host species, including Apodemus spp., were recorded. In addition, unlike most previous studies, different tissues were sampled and compared to assess their suitability for orthohantavirus screening and possible tissue tropism. Our data suggest possible virus-specific tissue tropism in rodent hosts. TULV was most commonly detected in the lung tissue, whereas KURV was more common in the liver, spleen, and brain. Moreover, Seewis and Asikkala viruses were detected in randomly found common shrews (Sorex araneus). In conclusion, we have demonstrated the presence of human-pathogenic KURV and the potentially pathogenic TULV in their typical hosts as well as their spillover to atypical host species belonging to another family. Furthermore, we suggest the possibility of virus-specific tissue tropism of orthohantaviruses in their natural hosts. IMPORTANCE Orthohantaviruses (genus Orthohantavirus, family Hantaviridae) are a diverse group of globally distributed viruses that are closely associated with their natural hosts. Some orthohantaviruses are capable of infecting humans and causing severe disease. Orthohantaviruses are considered emerging pathogens due to their ever-increasing diversity and increasing numbers of disease cases. We report the detection of four different orthohantaviruses in rodents and shrews in the Czech Republic. Most viruses were found in their typical hosts, Kurkino virus (KURV) in striped field mice (Apodemus agrarius), Tula virus (TULV) in common voles (Microtus arvalis), and Seewis virus in common shrews (Sorex araneus). Nevertheless, spillover infections of atypical host species were also recorded for KURV, TULV, and another shrew-borne orthohantavirus, Asikkala virus. In addition, indications of virus-specific patterns of tissue tropism were observed. Our results highlight the circulation of several orthohantaviruses, including KURV, which is pathogenic to humans, among rodents and shrews in the Czech Republic.

Dataset Information

Peripheral immune responses to filoviruses in a reservoir versus spillover hosts reveal transcriptional correlates of disease.

Publications

Peripheral immune responses to filoviruses in a reservoir versus spillover hosts reveal transcriptional correlates of disease.

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