Oropouche orthobunyavirus infection is mediated by the cellular host factor Lrp1
Oropouche orthobunyavirus (OROV; Peribunyaviridae) is a mosquito-transmitted virus that causes widespread human febrile illness in South America, with occasional progression to neurologic effects. Host factors mediating the cellular entry of OROV are undefined. Here, we show that OROV uses the host...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2022-08, Vol.119 (33), p.1-9 |
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| creator | Schwarz, Madeline M. Price, David A. Ganaie, Safder S. Feng, Annie Mishra, Nawneet Hoehl, Ryan M. Fatma, Farheen Stubbs, Sarah H. Whelan, Sean P. J. Cui, Xiaoxia Egawa, Takeshi Leung, Daisy W. Amarasinghe, Gaya K. Hartman, Amy L. |
| description | Oropouche orthobunyavirus (OROV; Peribunyaviridae) is a mosquito-transmitted virus that causes widespread human febrile illness in South America, with occasional progression to neurologic effects. Host factors mediating the cellular entry of OROV are undefined. Here, we show that OROV uses the host protein low-density lipoprotein—related protein 1 (Lrp1) for efficient cellular infection. Cells from evolutionarily distinct species lacking Lrp1 were less permissive to OROV infection than cells with Lrp1. Treatment of cells with either the high-affinity Lrp1 ligand receptor-associated protein (RAP) or recombinant ectodomain truncations of Lrp1 significantly reduced OROV infection. In addition, chimeric vesicular stomatitis virus (VSV) expressing OROV glycoproteins (VSV-OROV) bound to the Lrp1 ectodomain in vitro. Furthermore, we demonstrate the biological relevance of the OROV-Lrp1 interaction in a proof-of-concept mouse study in which treatment of mice with RAP at the time of infection reduced tissue viral load and promoted survival from an otherwise lethal infection. These results with OROV, along with the recent finding of Lrp1 as an entry factor for Rift Valley fever virus, highlight the broader significance of Lrp1 in cellular infection by diverse bunyaviruses. Shared strategies for entry, such as the critical function of Lrp1 defined here, provide a foundation for the development of pan-bunyaviral therapeutics. |
| doi_str_mv | 10.1073/pnas.2204706119 |
| format | Article |
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J. ; Cui, Xiaoxia ; Egawa, Takeshi ; Leung, Daisy W. ; Amarasinghe, Gaya K. ; Hartman, Amy L.</creator><creatorcontrib>Schwarz, Madeline M. ; Price, David A. ; Ganaie, Safder S. ; Feng, Annie ; Mishra, Nawneet ; Hoehl, Ryan M. ; Fatma, Farheen ; Stubbs, Sarah H. ; Whelan, Sean P. J. ; Cui, Xiaoxia ; Egawa, Takeshi ; Leung, Daisy W. ; Amarasinghe, Gaya K. ; Hartman, Amy L.</creatorcontrib><description>Oropouche orthobunyavirus (OROV; Peribunyaviridae) is a mosquito-transmitted virus that causes widespread human febrile illness in South America, with occasional progression to neurologic effects. Host factors mediating the cellular entry of OROV are undefined. Here, we show that OROV uses the host protein low-density lipoprotein—related protein 1 (Lrp1) for efficient cellular infection. Cells from evolutionarily distinct species lacking Lrp1 were less permissive to OROV infection than cells with Lrp1. Treatment of cells with either the high-affinity Lrp1 ligand receptor-associated protein (RAP) or recombinant ectodomain truncations of Lrp1 significantly reduced OROV infection. In addition, chimeric vesicular stomatitis virus (VSV) expressing OROV glycoproteins (VSV-OROV) bound to the Lrp1 ectodomain in vitro. Furthermore, we demonstrate the biological relevance of the OROV-Lrp1 interaction in a proof-of-concept mouse study in which treatment of mice with RAP at the time of infection reduced tissue viral load and promoted survival from an otherwise lethal infection. These results with OROV, along with the recent finding of Lrp1 as an entry factor for Rift Valley fever virus, highlight the broader significance of Lrp1 in cellular infection by diverse bunyaviruses. Shared strategies for entry, such as the critical function of Lrp1 defined here, provide a foundation for the development of pan-bunyaviral therapeutics.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2204706119</identifier><identifier>PMID: 35939689</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Sciences ; Bunyaviridae Infections - metabolism ; Bunyaviridae Infections - virology ; Coccidioidomycosis ; Disease transmission ; Drug development ; Gene Knockout Techniques ; Glycoproteins ; Humans ; Infections ; Low Density Lipoprotein Receptor-Related Protein-1 - genetics ; Low Density Lipoprotein Receptor-Related Protein-1 - metabolism ; Mice ; Orthobunyavirus - physiology ; Proteins ; Rift Valley fever ; South America ; Stomatitis ; Vector-borne diseases ; Viral diseases ; Virus Internalization ; Viruses</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2022-08, Vol.119 (33), p.1-9</ispartof><rights>Copyright © 2022 the Author(s)</rights><rights>Copyright National Academy of Sciences Aug 16, 2022</rights><rights>Copyright © 2022 the Author(s). Published by PNAS. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-f39c223dcb2de3b01458787bd7d4df6854f2e8f048c683ae9c6b3ef779e2268d3</citedby><cites>FETCH-LOGICAL-c443t-f39c223dcb2de3b01458787bd7d4df6854f2e8f048c683ae9c6b3ef779e2268d3</cites><orcidid>0000-0002-3073-7332 ; 0000-0001-7489-1051 ; 0000-0002-7189-9557 ; 0000-0003-1564-8590 ; 0000-0002-3261-191X ; 0000-0002-0857-2973 ; 0000-0002-6807-9670 ; 0000-0002-9038-4655 ; 0000-0002-9014-6577</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9388146/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9388146/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27915,27916,53782,53784</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35939689$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Schwarz, Madeline M.</creatorcontrib><creatorcontrib>Price, David A.</creatorcontrib><creatorcontrib>Ganaie, Safder S.</creatorcontrib><creatorcontrib>Feng, Annie</creatorcontrib><creatorcontrib>Mishra, Nawneet</creatorcontrib><creatorcontrib>Hoehl, Ryan M.</creatorcontrib><creatorcontrib>Fatma, Farheen</creatorcontrib><creatorcontrib>Stubbs, Sarah H.</creatorcontrib><creatorcontrib>Whelan, Sean P. J.</creatorcontrib><creatorcontrib>Cui, Xiaoxia</creatorcontrib><creatorcontrib>Egawa, Takeshi</creatorcontrib><creatorcontrib>Leung, Daisy W.</creatorcontrib><creatorcontrib>Amarasinghe, Gaya K.</creatorcontrib><creatorcontrib>Hartman, Amy L.</creatorcontrib><title>Oropouche orthobunyavirus infection is mediated by the cellular host factor Lrp1</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Oropouche orthobunyavirus (OROV; Peribunyaviridae) is a mosquito-transmitted virus that causes widespread human febrile illness in South America, with occasional progression to neurologic effects. Host factors mediating the cellular entry of OROV are undefined. Here, we show that OROV uses the host protein low-density lipoprotein—related protein 1 (Lrp1) for efficient cellular infection. Cells from evolutionarily distinct species lacking Lrp1 were less permissive to OROV infection than cells with Lrp1. Treatment of cells with either the high-affinity Lrp1 ligand receptor-associated protein (RAP) or recombinant ectodomain truncations of Lrp1 significantly reduced OROV infection. In addition, chimeric vesicular stomatitis virus (VSV) expressing OROV glycoproteins (VSV-OROV) bound to the Lrp1 ectodomain in vitro. Furthermore, we demonstrate the biological relevance of the OROV-Lrp1 interaction in a proof-of-concept mouse study in which treatment of mice with RAP at the time of infection reduced tissue viral load and promoted survival from an otherwise lethal infection. These results with OROV, along with the recent finding of Lrp1 as an entry factor for Rift Valley fever virus, highlight the broader significance of Lrp1 in cellular infection by diverse bunyaviruses. 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J.</au><au>Cui, Xiaoxia</au><au>Egawa, Takeshi</au><au>Leung, Daisy W.</au><au>Amarasinghe, Gaya K.</au><au>Hartman, Amy L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oropouche orthobunyavirus infection is mediated by the cellular host factor Lrp1</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2022-08-16</date><risdate>2022</risdate><volume>119</volume><issue>33</issue><spage>1</spage><epage>9</epage><pages>1-9</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Oropouche orthobunyavirus (OROV; Peribunyaviridae) is a mosquito-transmitted virus that causes widespread human febrile illness in South America, with occasional progression to neurologic effects. Host factors mediating the cellular entry of OROV are undefined. Here, we show that OROV uses the host protein low-density lipoprotein—related protein 1 (Lrp1) for efficient cellular infection. Cells from evolutionarily distinct species lacking Lrp1 were less permissive to OROV infection than cells with Lrp1. Treatment of cells with either the high-affinity Lrp1 ligand receptor-associated protein (RAP) or recombinant ectodomain truncations of Lrp1 significantly reduced OROV infection. In addition, chimeric vesicular stomatitis virus (VSV) expressing OROV glycoproteins (VSV-OROV) bound to the Lrp1 ectodomain in vitro. Furthermore, we demonstrate the biological relevance of the OROV-Lrp1 interaction in a proof-of-concept mouse study in which treatment of mice with RAP at the time of infection reduced tissue viral load and promoted survival from an otherwise lethal infection. These results with OROV, along with the recent finding of Lrp1 as an entry factor for Rift Valley fever virus, highlight the broader significance of Lrp1 in cellular infection by diverse bunyaviruses. 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| subjects | Animals Biological Sciences Bunyaviridae Infections - metabolism Bunyaviridae Infections - virology Coccidioidomycosis Disease transmission Drug development Gene Knockout Techniques Glycoproteins Humans Infections Low Density Lipoprotein Receptor-Related Protein-1 - genetics Low Density Lipoprotein Receptor-Related Protein-1 - metabolism Mice Orthobunyavirus - physiology Proteins Rift Valley fever South America Stomatitis Vector-borne diseases Viral diseases Virus Internalization Viruses |
| title | Oropouche orthobunyavirus infection is mediated by the cellular host factor Lrp1 |
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