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Volume 103, Issue 10

Identification of novel orthonairoviruses from rodents and shrews in Gabon, Central Africa Open Access

Abstract

In Africa, several emerging zoonotic viruses have been transmitted from small mammals such as rodents and shrews to humans. Although no clinical cases of small mammal-borne viral diseases have been reported in Central Africa, potential zoonotic viruses have been identified in rodents in the region. Therefore, we hypothesized that there may be unrecognized zoonotic viruses circulating in small mammals in Central Africa. Here, we investigated viruses that have been maintained among wild small mammals in Gabon to understand their potential risks to humans. We identified novel orthonairoviruses in 24.6 % of captured rodents and shrews from their kidney total RNA samples. Phylogenetic analysis revealed that the novel viruses, Lamusara virus (LMSV) and Lamgora virus, were closely related to Erve virus, which was previously identified in shrews of the genus and has been suspected to cause neuropathogenic diseases in humans. Moreover, we show that the LMSV ovarian tumour domain protease, one of the virulence determination factors of orthonairoviruses, suppressed interferon signalling in human cells, suggesting the possible human pathogenicity of this virus. Taken together, our study demonstrates the presence of novel orthonairoviruses that may pose unrecognized risks of viral disease transmission in Gabon.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Gabon , novel virus , Orthonairovirus , small mammals , surveillance and virus screening
Funding
This study was supported by the:
  • Japan Society for the Promotion of Science (Award 21K10415)
    • Principle Award Recipient: HarukaAbe
  • Japan Society for the Promotion of Science (Award JP17KK0170)
    • Principle Award Recipient: YoheiKurosaki
  • JICA (Award JP20jm0110013)
    • Principle Award Recipient: JiroYasuda
  • the Japan Agency for Medical Research and Development (Award JP20jm0210072)
    • Principle Award Recipient: JiroYasuda
  • the Japan Agency for Medical Research and Development (Award JP20jm0110013)
    • Principle Award Recipient: JiroYasuda
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2022-10-10
2024-04-30
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References

  1. Meerburg BG, Singleton GR, Kijlstra A. Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 2009; 35:221–270 [View Article] [PubMed]
     [Google Scholar]
  2. Garrison AR, Alkhovsky [Альховский Сергей Владимирович] SV, Avšič-Županc T, Bente DA, Bergeron É et al. ICTV virus taxonomy profile: Nairoviridae. J Gen Virol 2020; 101:798–799 [View Article]
     [Google Scholar]
  3. Kuhn JH, Wiley MR, Rodriguez SE, Bào Y, Prieto K et al. Genomic characterization of the genus Nairovirus (Family Bunyaviridae). Viruses 2016; 8:E164 [View Article] [PubMed]
     [Google Scholar]
  4. Bente DA, Forrester NL, Watts DM, McAuley AJ, Whitehouse CA et al. Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res 2013; 100:159–189 [View Article] [PubMed]
     [Google Scholar]
  5. Marczinke BI, Nichol ST. Nairobi sheep disease virus, an important tick-borne pathogen of sheep and goats in Africa, is also present in Asia. Virology 2002; 303:146–151 [View Article] [PubMed]
     [Google Scholar]
  6. Brès P, Cornet M, Robin Y. The Bandia Forest virus (IPD-A 611), a new arbovirus prototype isolated in Senegal. Ann Inst Pasteur (Paris) 1967; 113:739–747
     [Google Scholar]
  7. Walker PJ, Widen SG, Firth C, Blasdell KR, Wood TG et al. Genomic characterization of Yogue, Kasokero, Issyk-Kul, Keterah, Gossas, and Thiafora viruses: nairoviruses naturally infecting bats, shrews, and ticks. Am J Trop Med Hyg 2015; 93:1041–1051 [View Article] [PubMed]
     [Google Scholar]
  8. Kenmoe S, Tchatchouang S, Ebogo-Belobo JT, Ka’e AC, Mahamat G et al. Systematic review and meta-analysis of the epidemiology of Lassa virus in humans, rodents and other mammals in sub-Saharan Africa. PLoS Negl Trop Dis 2020; 14:e0008589 [View Article] [PubMed]
     [Google Scholar]
  9. Mylne AQN, Pigott DM, Longbottom J, Shearer F, Duda KA et al. Mapping the zoonotic niche of Lassa fever in Africa. Trans R Soc Trop Med Hyg 2015; 109:483–492 [View Article] [PubMed]
     [Google Scholar]
  10. Kronmann KC, Nimo-Paintsil S, Guirguis F, Kronmann LC, Bonney K et al. Two novel arenaviruses detected in pygmy mice, Ghana. Emerg Infect Dis 2013; 19:1832–1835 [View Article] [PubMed]
     [Google Scholar]
  11. Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V et al. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 2006; 12:838–840 [View Article] [PubMed]
     [Google Scholar]
  12. Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V et al. Novel hantavirus sequences in Shrew, Guinea. Emerg Infect Dis 2007; 13:520–522 [View Article] [PubMed]
     [Google Scholar]
  13. Gonzalez JP, McCormick JB, Saluzzo JF, Herve JP, Georges AJ et al. An arenavirus isolated from wild-caught rodents (Pramys species) in the Central African Republic. Intervirology 1983; 19:105–112 [View Article] [PubMed]
     [Google Scholar]
  14. Gonzalez JP, McCormick JB, Saluzzo JF, Georges AJ. Les fièvres hémorragiques africaines d’origine virale: contribution à leur étude en République Centrafricaine. Cahiers ORSTOM Série Entomologie Médicale et Parasitologie 1983; 21:119–130
     [Google Scholar]
  15. Těšíková J, Krásová J, Goüy de Bellocq J. Multiple mammarenaviruses circulating in angolan rodents. Viruses 2021; 13:982 [View Article]
     [Google Scholar]
  16. N’ Dilimabaka N, Berthet N, Rougeron V, Mangombi JB, Durand P et al. Evidence of lymphocytic choriomeningitis virus (LCMV) in domestic mice in Gabon: risk of emergence of LCMV encephalitis in Central Africa. J Virol 2015; 89:1456–1460 [View Article] [PubMed]
     [Google Scholar]
  17. Ushijima Y, Abe H, Ozeki T, Ondo GN, Mbadinga MJVM et al. Identification of potential novel hosts and the risk of infection with lymphocytic choriomeningitis virus in humans in Gabon, Central Africa. Int J Infect Dis 2021; 105:452–459 [View Article] [PubMed]
     [Google Scholar]
  18. Heinemann P, Tia M, Alabi A, Anon J-C, Auste B et al. Human infections by Non-Rodent-Associated hantaviruses in Africa. J Infect Dis 2016; 214:1507–1511 [View Article] [PubMed]
     [Google Scholar]
  19. Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A et al. Molecular surveillance and phylogenetic analysis of Old World arenaviruses in Zambia. J Gen Virol 2012; 93:2247–2251 [View Article] [PubMed]
     [Google Scholar]
  20. Madai M, Horváth G, Herczeg R, Somogyi B, Zana B et al. Effectiveness regarding hantavirus detection in rodent tissue samples and urine. Viruses 2021; 13:570 [View Article] [PubMed]
     [Google Scholar]
  21. Tan Z, Yu H, Xu L, Zhao Z, Zhang P et al. Virome profiling of rodents in Xinjiang Uygur Autonomous Region, China: isolation and characterization of a new strain of Wenzhou virus. Virology 2019; 529:122–134 [View Article] [PubMed]
     [Google Scholar]
  22. Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A et al. Novel arenavirus, Zambia. Emerg Infect Dis 2011; 17:1921–1924 [View Article] [PubMed]
     [Google Scholar]
  23. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article] [PubMed]
     [Google Scholar]
  24. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
     [Google Scholar]
  25. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
     [Google Scholar]
  26. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:vev003 [View Article] [PubMed]
     [Google Scholar]
  27. Hirano M, Sakurai Y, Urata S, Kurosaki Y, Yasuda J et al. A screen of FDA-approved drugs with minigenome identified tigecycline as an antiviral targeting nucleoprotein of Crimean-Congo hemorrhagic fever virus. Antiviral Res 2022; 200:105276 [View Article] [PubMed]
     [Google Scholar]
  28. Zadeh VR, Urata S, Sakaguchi M, Yasuda J. Human BST-2/tetherin inhibits Junin virus release from host cells and its inhibition is partially counteracted by viral nucleoprotein. J Gen Virol 2020; 101:573–586 [View Article] [PubMed]
     [Google Scholar]
  29. Walker PJ, Widen SG, Wood TG, Guzman H, Tesh RB et al. A global genomic characterization of nairoviruses identifies nine discrete genogroups with distinctive structural characteristics and Host-Vector Associations. Am J Trop Med Hyg 2016; 94:1107–1122 [View Article] [PubMed]
     [Google Scholar]
  30. Chastel C, Main AJ, Richard P, Le Lay G, Legrand-Quillien MC et al. Erve virus, a probable member of Bunyaviridae family isolated from shrews (Crocidura russula) in France. Acta Virol 1989; 33:270–280 [PubMed]
     [Google Scholar]
  31. Chamberlain J, Cook N, Lloyd G, Mioulet V, Tolley H et al. Co-evolutionary patterns of variation in small and large RNA segments of Crimean-Congo hemorrhagic fever virus. J Gen Virol 2005; 86:3337–3341 [View Article] [PubMed]
     [Google Scholar]
  32. Lukashev ANY. Evidence for recombination in Crimean-Congo hemorrhagic fever virus. J Gen Virol 2005; 86:2333–2338 [View Article] [PubMed]
     [Google Scholar]
  33. Frias-Staheli N, Giannakopoulos NV, Kikkert M, Taylor SL, Bridgen A et al. Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2007; 2:404–416 [View Article] [PubMed]
     [Google Scholar]
  34. Deaton MK, Dzimianski JV, Daczkowski CM, Whitney GK, Mank NJ et al. Biochemical and structural insights into the preference of nairoviral DeISGylases for Interferon-Stimulated gene product 15 originating from certain species. J Virol 2016; 90:8314–8327 [View Article]
     [Google Scholar]
  35. Dzimianski JV, Scholte FEM, Williams IL, Langley C, Freitas BT et al. Determining the molecular drivers of species-specific interferon-stimulated gene product 15 interactions with nairovirus ovarian tumor domain proteases. PLoS ONE 2019; 14:e0226415 [View Article] [PubMed]
     [Google Scholar]
  36. Altamura LA, Bertolotti-Ciarlet A, Teigler J, Paragas J, Schmaljohn CS et al. Identification of a novel C-terminal cleavage of Crimean-Congo hemorrhagic fever virus PreGN that leads to generation of an NSM protein. J Virol 2007; 81:6632–6642 [View Article] [PubMed]
     [Google Scholar]
  37. Vincent MJ, Sanchez AJ, Erickson BR, Basak A, Chretien M et al. Crimean-Congo hemorrhagic fever virus glycoprotein proteolytic processing by subtilase SKI-1. J Virol 2003; 77:8640–8649 [View Article] [PubMed]
     [Google Scholar]
  38. Sanchez AJ, Vincent MJ, Nichol ST. Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus. J Virol 2002; 76:7263–7275 [View Article] [PubMed]
     [Google Scholar]
  39. Freitas N, Enguehard M, Denolly S, Levy C, Neveu G et al. The interplays between Crimean-Congo hemorrhagic fever virus (CCHFV) M segment-encoded accessory proteins and structural proteins promote virus assembly and infectivity. PLoS Pathog 2020; 16:e1008850 [View Article] [PubMed]
     [Google Scholar]
  40. Guo Y, Wang W, Ji W, Deng M, Sun Y et al. Crimean-Congo hemorrhagic fever virus nucleoprotein reveals endonuclease activity in bunyaviruses. Proc Natl Acad Sci U S A 2012; 109:5046–5051 [View Article] [PubMed]
     [Google Scholar]
  41. Wang W, Liu X, Wang X, Dong H, Ma C et al. Structural and functional diversity of nairovirus-encoded nucleoproteins. J Virol 2015; 89:11740–11749 [View Article] [PubMed]
     [Google Scholar]
  42. Hewson R, Gmyl A, Gmyl L, Smirnova SE, Karganova G et al. Evidence of segment reassortment in Crimean-Congo haemorrhagic fever virus. J Gen Virol 2004; 85:3059–3070 [View Article]
     [Google Scholar]
  43. Burt FJ, Paweska JT, Ashkettle B, Swanepoel R. Genetic relationship in southern African Crimean-Congo haemorrhagic fever virus isolates: evidence for occurrence of reassortment. Epidemiol Infect 2009; 137:1302–1308 [View Article] [PubMed]
     [Google Scholar]
  44. Kajihara M, Simuunza M, Saasa N, Dautu G, Mori-Kajihara A et al. Serologic and molecular evidence for circulation of Crimean-Congo hemorrhagic fever virus in ticks and cattle in Zambia. PLoS Negl Trop Dis 2021; 15:e0009452 [View Article] [PubMed]
     [Google Scholar]
  45. Woessner R, Grauer MT, Langenbach J, Dobler G, Kroeger J et al. The Erve virus: possible mode of transmission and reservoir. Infection 2000; 28:164–166 [View Article] [PubMed]
     [Google Scholar]
  46. Skaug B, Chen ZJ. Emerging role of ISG15 in antiviral immunity. Cell 2010; 143:187–190 [View Article] [PubMed]
     [Google Scholar]
  47. Capodagli GC, Deaton MK, Baker EA, Lumpkin RJ, Pegan SD. Diversity of ubiquitin and ISG15 specificity among nairoviruses’ viral ovarian tumor domain proteases. J Virol 2013; 87:3815–3827 [View Article] [PubMed]
     [Google Scholar]
  48. Treib J, Dobler G, Haass A, von Blohn W, Strittmatter M et al. Thunderclap headache caused by Erve virus?. Neurology 1998; 50:509–511 [View Article] [PubMed]
     [Google Scholar]
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Identification of novel orthonairoviruses from rodents and shrews in Gabon, Central Africa
J. Gen. Virol. 103, 001796 (2022); https://doi.org/10.1099/jgv.0.001796
/content/journal/jgv/10.1099/jgv.0.001796
/content/journal/jgv/10.1099/jgv.0.001796
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