Cross reactivity of neutralizing antibodies to the encephalitic California Serogroup orthobunyaviruses varies by virus and genetic relatedness.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
12 08 2021
12 08 2021
Historique:
received:
20
05
2021
accepted:
15
07
2021
entrez:
13
8
2021
pubmed:
14
8
2021
medline:
16
11
2021
Statut:
epublish
Résumé
The California Serogroup (CSG) of Orthobunyaviruses comprises several viruses capable of causing neuroinvasive disease in humans, including La Crosse (LACV), Snowshoe Hare (SSHV), Tahyna (TAHV), Jamestown Canyon (JCV), and Inkoo (INKV) viruses. Diagnosis of specific CSG viruses is complicated by the high degree of antibody cross-reactivity between them, with laboratory standards requiring a fourfold higher titer of neutralizating antibody (NAb) activity to positively identify the etiologic virus. To help elucidate NAb relationships between neuroinvasive CSG viruses, we directly compared the cross-reactivity of NAb between LACV, SSHV, TAHV, JCV, and INKV. Mice were inoculated with individual viruses and the NAb activity of plasma samples was compared by plaque reduction neutralization tests against all five viruses. Overall, the results from these studies show that the CSG viruses induced high levels of NAb against the inoculum virus, and differing amounts of cross-reactive NAb against heterologous viruses. LACV, SSHV, and INKV elicited the highest amount of cross-reactive NAb. Interestingly, a fourfold difference in NAb titer between the inoculum virus and the other CSG viruses was not always observed. Thus, NAb titers, which are the gold-standard for diagnosing the etiologic agent for viral encephalitis, may not clearly differentiate between different CSG viruses.
Identifiants
pubmed: 34385513
doi: 10.1038/s41598-021-95757-2
pii: 10.1038/s41598-021-95757-2
pmc: PMC8361150
doi:
Substances chimiques
Antibodies, Neutralizing
0
Antibodies, Viral
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
16424Informations de copyright
© 2021. The Author(s).
Références
Evans, A. B. & Peterson, K. E. Throw out the map: Neuropathogenesis of the globally expanding California Serogroup of orthobunyaviruses. Viruses 11, 794. https://doi.org/10.3390/v11090794 (2019).
doi: 10.3390/v11090794
pmcid: 6784171
Putkuri, N. et al. Acute human inkoo and chatanga virus infections, Finland. Emerg. Infect. Dis. 22, 810–817. https://doi.org/10.3201/eid2205.151015 (2016).
doi: 10.3201/eid2205.151015
pubmed: 27088268
pmcid: 4861510
Thompson, W. H., Kalfayan, B. & Anslow, R. O. Isolation of California encephalitis group virus from a fatal human illness. Am. J. Epidemiol. 81, 245–253. https://doi.org/10.1093/oxfordjournals.aje.a120512 (1965).
doi: 10.1093/oxfordjournals.aje.a120512
pubmed: 14261030
Fauvel, M. et al. California group virus encephalitis in three children from Quebec: Clinical and serologic findings. Can. Med. Assoc. J. 122, 60–62 (1980).
pubmed: 7363197
pmcid: 1801601
Grimstad, P. R., Shabino, C. L., Calisher, C. H. & Waldman, R. J. A case of encephalitis in a human associated with a serologic rise to Jamestown Canyon virus. Am. J. Trop. Med. Hyg. 31, 1238–1244. https://doi.org/10.4269/ajtmh.1982.31.1238 (1982).
doi: 10.4269/ajtmh.1982.31.1238
pubmed: 7149109
Blitvich, B. J. et al. Identification of a novel subtype of South River virus (family Bunyaviridae). Arch. Virol. 157, 1205–1209. https://doi.org/10.1007/s00705-012-1280-4 (2012).
doi: 10.1007/s00705-012-1280-4
pubmed: 22411100
pmcid: 3634354
Hughes, H. R., Lanciotti, R. S., Blair, C. D. & Lambert, A. J. Full genomic characterization of California serogroup viruses, genus Orthobunyavirus, family Peribunyaviridae including phylogenetic relationships. Virology 512, 201–210. https://doi.org/10.1016/j.virol.2017.09.022 (2017).
doi: 10.1016/j.virol.2017.09.022
pubmed: 28985574
Rogers, M. B. et al. Characterization of five unclassified orthobunyaviruses (Bunyaviridae) from Africa and the Americas. J. Gen. Virol. 98, 2258–2266. https://doi.org/10.1099/jgv.0.000899 (2017).
doi: 10.1099/jgv.0.000899
pubmed: 28885138
pmcid: 5817192
Sather, G. E. & Hammon, W. M. Antigenic patterns within the California-encephalitis-virus group. Am. J. Trop. Med. Hyg. 16, 548–557. https://doi.org/10.4269/ajtmh.1967.16.548 (1967).
doi: 10.4269/ajtmh.1967.16.548
pubmed: 4952153
Karabatsos, C. H. C. A. N. in The Arboviruses: Epidemiology and Ecology Vol. 1 (ed. Thomas P. Monath) Ch. 2, (CRC Press, Taylor & Francis Group, 1988).
Brummer-Korvenkontio, M. et al. Arboviruses in Finland. IV. Isolation and characterization of Inkoo virus, a Finnish representative of the California group. Am. J. Trop. Med. Hyg. 22, 404–413 (1973).
doi: 10.4269/ajtmh.1973.22.404
Mestas, J. & Hughes, C. C. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172, 2731–2738. https://doi.org/10.4049/jimmunol.172.5.2731 (2004).
doi: 10.4049/jimmunol.172.5.2731
pubmed: 14978070
Evans, A. B., Winkler, C. W. & Peterson, K. E. Differences in neuropathogenesis of encephalitic California Serogroup viruses. Emerg. Infect. Dis. 25, 728–738. https://doi.org/10.3201/eid2504.181016 (2019).
doi: 10.3201/eid2504.181016
pubmed: 30882310
pmcid: 6433036
Elliott, R. M. Orthobunyaviruses: Recent genetic and structural insights. Nat. Rev. Microbiol. 12, 673–685. https://doi.org/10.1038/nrmicro3332 (2014).
doi: 10.1038/nrmicro3332
pubmed: 25198140
Hellert, J. et al. Orthobunyavirus spike architecture and recognition by neutralizing antibodies. Nat. Commun. 10, 879. https://doi.org/10.1038/s41467-019-08832-8 (2019).
doi: 10.1038/s41467-019-08832-8
pubmed: 30787296
pmcid: 6382863
Kingsford, L. Enhanced neutralization of La Crosse virus by the binding of specific pairs of monoclonal antibodies to the G1 glycoprotein. Virology 136, 265–273. https://doi.org/10.1016/0042-6822(84)90163-6 (1984).
doi: 10.1016/0042-6822(84)90163-6
pubmed: 6205500
Pastula, D. M. et al. Jamestown canyon virus disease in the United States-2000-2013. Am. J. Trop. Med. Hyg. 93, 384–389. https://doi.org/10.4269/ajtmh.15-0196 (2015).
doi: 10.4269/ajtmh.15-0196
pubmed: 26033022
pmcid: 4530766
Webster, D. et al. California Serogroup virus infection associated with encephalitis and cognitive decline, Canada, 2015. Emerg. Infect. Dis. 23, 1423–1424. https://doi.org/10.3201/eid2308.170239 (2017).
doi: 10.3201/eid2308.170239
pubmed: 28726628
pmcid: 5547809
Ludwig, G. V., Israel, B. A., Christensen, B. M., Yuill, T. M. & Schultz, K. T. Monoclonal antibodies directed against the envelope glycoproteins of La Crosse virus. Microb. Pathog. 11, 411–421. https://doi.org/10.1016/0882-4010(91)90037-b (1991).
doi: 10.1016/0882-4010(91)90037-b
pubmed: 1795631
Kingsford, L. & Hill, D. W. The effect of proteolytic cleavage of La Crosse virus G1 glycoprotein on antibody neutralization. J. Gen. Virol. 64(Pt 10), 2147–2156. https://doi.org/10.1099/0022-1317-64-10-2147 (1983).
doi: 10.1099/0022-1317-64-10-2147
pubmed: 6352863
L’Vov, S. D. et al. Distribution of viruses from the Californian encephalitis serogroup (Bunyaviridae, Bunyavirus) in the northern expanses of Russia. Vopr. Virusol. 42, 229–235 (1997).
pubmed: 9424850
Putkuri, N. et al. Isolation and characterization of a California encephalitis serogroup orthobunyavirus from Finnish mosquitoes. Infect. Genet. Evol. 22, 164–173. https://doi.org/10.1016/j.meegid.2014.01.023 (2014).
doi: 10.1016/j.meegid.2014.01.023
pubmed: 24480054
Bennett, R. S., Gresko, A. K., Nelson, J. T., Murphy, B. R. & Whitehead, S. S. A recombinant chimeric La Crosse virus expressing the surface glycoproteins of Jamestown Canyon virus is immunogenic and protective against challenge with either parental virus in mice or monkeys. J. Virol. 86, 420–426. https://doi.org/10.1128/JVI.02327-10 (2012).
doi: 10.1128/JVI.02327-10
pubmed: 22013033
pmcid: 3255902
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12. https://doi.org/10.14806/ej.17.1.200 (2011).
doi: 10.14806/ej.17.1.200
Hannon, G. J. FASTX-Toolkit. (2010).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. https://doi.org/10.1038/nmeth.1923 (2012).
doi: 10.1038/nmeth.1923
pubmed: 22388286
pmcid: 3322381
Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience https://doi.org/10.1093/gigascience/giab008 (2021).
doi: 10.1093/gigascience/giab008
pubmed: 33594436
pmcid: 7931820