1921
Volume 94, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract

Nairoviruses are primarily tick-borne bunyaviruses, some of which are known to cause mild-to-severe febrile illness in humans or livestock. We describe the genome sequences of 11 poorly characterized nairoviruses that have ecological associations with either birds (Farallon, Punta Salinas, Sapphire II, Zirqa, Avalon, Clo Mor, Taggert, and Abu Hammad viruses), rodents (Qalyub and Bandia viruses), or camels (Dera Ghazi Khan virus). Global phylogenetic analyses of proteins encoded in the L, M, and S RNA segments of these and 20 other available nairovirus genomes identified nine well-supported genogroups (Nairobi sheep disease, Thiafora, Sakhalin, Keterah, Qalyub, Kasokero, Dera Ghazi Khan, Hughes, and Tamdy). Genogroup-specific structural variations were evident, particularly in the M segment encoding a polyprotein from which virion envelope glycoproteins (Gn and Gc) are generated by proteolytic processing. Structural variations include the extension, abbreviation, or absence sequences encoding an O-glycosylated mucin-like protein in the N-terminal domain, distinctive patterns of conserved cysteine residues in the GP38-like domain, insertion of sequences encoding a double-membrane-spanning protein (NSm) between the Gn and Gc domains, and the presence of an alternative long open reading frame encoding a viroporin-like transmembrane protein (Gx). We also observed strong genogroup-specific associations with categories of hosts and tick vectors.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.15-0917
2016-05-04
2017-09-21
Loading full text...

Full text loading...

/deliver/fulltext/14761645/94/5/1107.html?itemId=/content/journals/10.4269/ajtmh.15-0917&mimeType=html&fmt=ahah

References

  1. Lasecka L, Baron MD, , 2014. The molecular biology of nairoviruses, an emerging group of tick-borne arboviruses. Arch Virol 159: 12491265.[Crossref]
  2. Treib J, Dobler G, Haass A, von Blohn W, Strittmatter M, Pindur G, Froesner G, Schimrigk K, , 1998. Thunderclap headache caused by Erve virus? Neurology 50: 509511.[Crossref]
  3. L'vov DK, Kostiukov MA, Daniiarov OA, Tukhtaev TM, Sherikov BK, , 1984. Outbreak of arbovirus infection in the Tadzhik SSR due to the Issyk-kul virus (Issyk-kul fever). Vopr Virusol 29: 8992.
  4. Kalunda M, Mukwaya LG, Mukuye A, Lule M, Sekyalo E, Wright J, Casals J, , 1986. Kasokero virus: a new human pathogen from bats (Rousettus aegyptiacus) in Uganda. Am J Trop Med Hyg 35: 387392.
  5. Burt FJ, Spencer DC, Leman PA, Patterson B, Swanepoel R, , 1996. Investigation of tick-borne viruses as pathogens of humans in South Africa and evidence of Dugbe virus infection in a patient with prolonged thrombocytopenia. Epidemiol Infect 116: 353361.[Crossref]
  6. Bente DA, Forrester NL, Watts DM, McAuley AJ, Whitehouse CA, Bray M, , 2013. Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome, and genetic diversity. Antiviral Res 100: 159189.[Crossref]
  7. Ince Y, Yasa C, Metin M, Sonmez M, Meram E, Benkli B, Ergonul O, , 2014. Crimean-Congo hemorrhagic fever infections reported by ProMED. Int J Infect Dis 26: 4446.[Crossref]
  8. Marczinke BI, Nichol ST, , 2002. Nairobi sheep disease virus, an important tick-borne pathogen of sheep and goats in Africa, is also present in Asia. Virology 303: 146151.[Crossref]
  9. Gong S, He B, Wang Z, Shang L, Wei F, Liu Q, Tu C, , 2015. Nairobi sheep disease virus RNA in Ixodid ticks, China, 2013. Emerg Infect Dis 21: 718720.[Crossref]
  10. Walker PJ, Widen SG, Firth C, Blasdell KR, Wood TG, Travassos da Rosa AP, Guzman H, Tesh RB, Vasilakis N, , 2015. Genomic characterization of Yogue, Kasokero, Issyk-Kul, Keterah, Gossas, and Thiafora viruses: nairoviruses naturally infecting bats, shrews, and ticks. Am J Trop Med Hyg 93: 10411051.[Crossref]
  11. Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, Lundkvist A, Schmaljohn CS, Tesh RB, King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, , 2012. Family Bunyaviridae . , eds. Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses. Amsterdam, The Netherlands: Elsevier Academic Press, 725741.
  12. Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ, , 2015. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. ELife 4: e05378.
  13. Tokarz R, Williams SH, Sameroff S, Sanchez Leon M, Jain K, Lipkin WI, , 2014. Virome analysis of Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis ticks reveals novel highly divergent vertebrate and invertebrate viruses. J Virol 88: 1148011492.[Crossref]
  14. Clerx JP, Bishop DH, , 1981. Qalyub virus, a member of the newly proposed Nairovirus genus (Bunyavividae). Virology 108: 361372.[Crossref]
  15. Brès P, Cornet M, Robin Y, , 1967. Bandia Forest virus (IPD/A611), a new arbovirus isolated in Senegal. Ann Inst Pasteur (Paris) 113: 739747.
  16. Karabatsos N, , 1985. International Catalogue of Arboviruses Including Certain other Viruses of Vertebrates. San Antonio, TX: American Society for Tropical Medicine and Hygiene.
  17. Yunker CE, Clifford CM, Thomas LA, Cory J, George JE, , 1972. Isolation of viruses from swallow ticks, Argas cooleyi, in the southwestern United States. Acta Virol 16: 415421.
  18. Varma MG, Bowen ET, Simpson DI, Casals J, , 1973. Zirga virus, a new arbovirus isolated from bird-infesting ticks. Nature 244: 452.[Crossref]
  19. Converse JD, Moussa MI, Easton ER, Casals J, , 1981. Punta Salinas virus (Hughes group) from Argas arboreus (Ixodoidea: Argasidae) in Tanzania. Trans R Soc Trop Med Hyg 75: 755756.[Crossref]
  20. Radovsky FJ, Stiller D, Johnson HN, Clifford CM, , 1967. Descriptive notes on Ornithodoros ticks from gull nests on Farallon Islands and isolation of a variant of Hughes virus. J Parasitol 53: 890892.[Crossref]
  21. Gould EA, Chanas AC, Buckley A, Varma MG, , 1983. Immunofluorescence studies on the antigenic interrelationships of the Hughes virus serogroup (genus Nairovirus) and identification of a new strain. J Gen Virol 64: 739742.[Crossref]
  22. Main AJ, Downs WG, Shope RE, Wallis RC, , 1976. Avalon and Clo Mor: two new Sakhalin group viruses from the North Atlantic. J Med Entomol 13: 309315.[Crossref]
  23. Doherty RL, Carley JG, Murray MD, Main AJ, Kay BH, Domrow R, , 1975. Isolation of arboviruses (Kemerovo group, Sakhalin group) from Ixodes uriae collected at Macquarie Island, Southern Ocean. Am J Trop Med Hyg 24: 521526.
  24. Begum F, Wisseman CL, Jr Casals J, , 1970. Tick-borne viruses of west Pakistan. III. Dera Ghazi Khan virus, a new agent isolated from Hyalomma dromedarii ticks in the D. G. Khan District of West Pakistan. Am J Epidemiol 92: 195196.[Crossref]
  25. Darwish MA, Imam IZ, Omar FM, , 1976. Complement-fixing antibodies against Abu Hammad and Abu Mina viruses in mammalian sera from Egypt. J Egypt Pub Hlth Assoc 51: 5154.
  26. Casals J, Tignor GH, , 1980. The Nairovirus genus: serological relationships. Intervirology 14: 144147.[Crossref]
  27. Bolger AM, Lohse M, Usadel B, , 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 21142120.[Crossref]
  28. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I, , 2009. ABySS: a parallel assembler for short read sequence data. Genome Res 19: 11171123.[Crossref]
  29. Langmead B, Salzberg SL, , 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357359.[Crossref]
  30. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP, , 2011. Integrative genomics viewer. Nat Biotechnol 29: 2426.[Crossref]
  31. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, , 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 27252729.[Crossref]
  32. Talavera G, Castresana J, , 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564577.[Crossref]
  33. L'vov DK, Al'khovskii SV, Shchelkanov M, Shchetinin AM, Aristova VA, Morozova TN, Gitel'man AK, Deriabin PG, Botikov AG, , 2014. Taxonomic status of the Chim virus (CHIMV) (Bunyaviridae, Nairovirus, Qalyub group) isolated from the Ixodidae and Argasidae ticks collected in the great gerbil (Rhombomys opimus Lichtenstein, 1823) (Muridae, Gerbillinae) burrows in Uzbekistan and Kazakhstan [in Russian]. Vopr Virusol 59: 1823.
  34. L'vov DK, Al'khovskii SV, Shchelkanov M, Shchetinin AM, Deriabin PG, Aristova VA, Gitel'man AK, Samokhvalov EI, Botikov AG, , 2014. Genetic characterization of the Sakhalin virus (SAKV), Paramushir virus (PMRV) (Sakhalin group, Nairovirus, Bunyaviridae), and Rukutama virus (RUKV) (Uukuniemi group, Phlebovirus, Bunyaviridae) isolated from the obligate parasites of the colonial sea-birds ticks Ixodes (Ceratixodes) uriae, White 1852 and I. signatus Birulya, 1895 in the water area of sea of the Okhotsk and Bering sea [in Russian]. Vopr Virusol 59: 1117.
  35. L'vov DK, Al'khovskii SV, Shchelkanov M, Shchetinin AM, Deriabin PG, Samokhvalov EI, Gitel'man AK, Botikov AG, , 2014. Genetic characterization of the Caspiy virus (CASV) (Bunyaviridae, Nairovirus) isolated from the Laridae (Vigors, 1825) and Sternidae (Bonaparte, 1838) birds and the Argasidae (Koch, 1844) ticks Ornithodoros capensis Neumann, 1901, in western and eastern coasts of the Caspian Sea [in Russian]. Vopr Virusol 59: 2429.
  36. L'vov DK, Al'khovskii SV, Shchelkanov M, Deriabin PG, Shchetinin AM, Samokhvalov EI, Aristova VA, Gitel'man AK, Botikov AG, , 2014. Genetic characterization of the Geran virus (GERV, Bunyaviridae, Nairovirus, Qalyub group) isolated from the ticks Ornithodoros verrucosus Olenev, Zasukhin and Fenyuk, 1934 (Argasidae) collected in the burrow of Meriones erythrourus Grey, 1842 in Azerbaijan [in Russian]. Vopr Virusol 59: 1318.
  37. L'vov DK, Al'khovskii SV, Shchelkanov M, Shchetinin AM, Aristova VA, Deriabin PG, Botikov AG, Gitel'man AK, , 2014. Taxonomy of previously unclassified Tamdy virus (TAMV) (Bunyaviridae, Nairovirus) isolated from the Hyalomma asiaticum asiaticum Schulce et Schlottke, 1929 (Ixodidae, Hyalomminae) in the Middle East and transcaucasia [in Russian]. Vopr Virusol 59: 1522.
  38. L'vov DK, Al'khovskii SV, Shchelkanov M, Shchetinin AM, Deriabin PG, Gitel'man AK, Aristova VA, Botikov AG, , 2014. Taxonomic status of the Burana virus (BURV) (Bunyaviridae, Nairovirus, Tamdy group) isolated from the ticks Haemaphysalis punctata Canestrini et Fanzago, 1877 and Haem. concinna Koch, 1844 (Ixodidae, Haemaphysalinae) in Kyrgyzstan [in Russian]. Vopr Virusol 59: 1015.
  39. Honig JE, Osborne JC, Nichol ST, , 2004. Crimean-Congo hemorrhagic fever virus genome L RNA segment and encoded protein. Virology 321: 2935.[Crossref]
  40. Aquino VH, Moreli ML, Moraes Figueiredo LT, , 2003. Analysis of Oropouche virus L protein amino acid sequence showed the presence of an additional conserved region that could harbour an important role for the polymerase activity. Arch Virol 148: 1928.[Crossref]
  41. Kinsella E, Martin SG, Grolla A, Czub M, Feldmann H, Flick R, , 2004. Sequence determination of the Crimean-Congo hemorrhagic fever virus L segment. Virology 321: 2328.[Crossref]
  42. Guo Y, Wang W, Ji W, Deng M, Sun Y, Zhou H, Yang C, Deng F, Wang H, Hu Z, Lou Z, Rao Z, , 2012. Crimean-Congo hemorrhagic fever virus nucleoprotein reveals endonuclease activity in bunyaviruses. Proc Natl Acad Sci USA 109: 50465051.[Crossref]
  43. Carter SD, Surtees R, Walter CT, Ariza A, Bergeron E, Nichol ST, Hiscox JA, Edwards TA, Barr JN, , 2012. Structure, function, and evolution of the Crimean-Congo hemorrhagic fever virus nucleocapsid protein. J Virol 86: 1091410923.[Crossref]
  44. Wang Y, Dutta S, Karlberg H, Devignot S, Weber F, Hao Q, Tan YJ, Mirazimi A, Kotaka M, , 2012. Structure of Crimean-Congo hemorrhagic fever virus nucleoprotein: superhelical homo-oligomers and the role of caspase-3 cleavage. J Virol 86: 1229412303.[Crossref]
  45. Wang W, Liu X, Wang X, Dong H, Ma C, Wang J, Liu B, Mao Y, Wang Y, Li T, Yang C, Guo Y, , 2015. Structural and functional diversity of nairovirus-encoded nucleoproteins. J Virol 89: 1174011749.[Crossref]
  46. Sanchez AJ, Vincent MJ, Erickson BR, Nichol ST, , 2006. Crimean-Congo hemorrhagic fever virus glycoprotein precursor is cleaved by furin-like and SKI-1 proteases to generate a novel 38-kilodalton glycoprotein. J Virol 80: 514525.[Crossref]
  47. Walker PJ, Widen SG, Firth C, Blasdell KR, Wood TG, Travassos da Rosa AP, Guzman H, Tesh RB, Vasilakis N, , 2015. Genomic characterization of Yogue, Kasokero, Issyk-Kul, Keterah, Gossas, and Thiafora viruses: nairoviruses naturally infecting bats, shrews, and ticks. Am J Trop Med Hyg 93: 10411051.[Crossref]
  48. Zeller HG, Karabatsos N, Calisher CH, Digoutte JP, Cropp CB, Murphy FA, Shope RE, , 1989. Electron microscopic and antigenic studies of uncharacterized viruses. II. Evidence suggesting the placement of viruses in the family Bunyaviridae . Arch Virol 108: 211227.[Crossref]
  49. L'vov DK, Sidorova GA, Gromashevsky VL, Kurbanov M, Skvoztsova LM, Gofman YP, Berezina LK, Klimenko SM, Zakharyan VA, Aristova VA, Neronov VM, , 1976. Virus “Tamdy”—a new arbovirus, isolated in the Uzbee S.S.R. and Turkmen S.S.R. from ticks Hyalomma asiaticum asiaticum Schulee et Schlottke, 1929, and Hyalomma plumbeum plumbeum Panzer, 1796. Arch Virol 51: 1521.[Crossref]
  50. Briese T, Calisher CH, Higgs S, , 2013. Viruses of the family Bunyaviridae: are all available isolates reassortants? Virology 446: 207216.[Crossref]
  51. Honig JE, Osborne JC, Nichol ST, , 2004. The high genetic variation of viruses of the genus Nairovirus reflects the diversity of their predominant tick hosts. Virology 318: 1016.[Crossref]
  52. Hewson R, Gmyl A, Gmyl L, Smirnova SE, Karganova G, Jamil B, Hasan R, Chamberlain J, Clegg C, , 2004. Evidence of segment reassortment in Crimean-Congo haemorrhagic fever virus. J Gen Virol 85: 30593070.[Crossref]
  53. Francica JR, Varela-Rohena A, Medvec A, Plesa G, Riley JL, Bates P, , 2010. Steric shielding of surface epitopes and impaired immune recognition induced by the Ebola virus glycoprotein. PLoS Pathog 6: e1001098.[Crossref]
  54. Yang ZY, Duckers HJ, Sullivan NJ, Sanchez A, Nabel EG, Nabel GJ, , 2000. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat Med 6: 886889.[Crossref]
  55. Simmons G, Wool-Lewis RJ, Baribaud F, Netter RC, Bates P, , 2002. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. J Virol 76: 25182528.[Crossref]
  56. Altgarde N, Eriksson C, Peerboom N, Phan-Xuan T, Moeller S, Schnabelrauch M, Svedhem S, Trybala E, Bergstrom T, Bally M, , 2015. Mucin-like region of herpes simplex virus type 1 attachment protein glycoprotein C (gC) modulates the virus-glycosaminoglycan interaction. J Biol Chem 290: 2147321485.[Crossref]
  57. Nieva JL, Madan V, Carrasco L, , 2012. Viroporins: structure and biological functions. Nat Rev Microbiol 10: 563574.[Crossref]
  58. Lama J, Carrasco L, , 1992. Expression of poliovirus nonstructural proteins in Escherichia coli cells. Modification of membrane permeability induced by 2B and 3A. J Biol Chem 267: 1593215937.
  59. Pinto LH, Holsinger LJ, Lamb RA, , 1992. Influenza virus M2 protein has ion channel activity. Cell 69: 517528.[Crossref]
  60. Griffin SD, Beales LP, Clarke DS, Worsfold O, Evans SD, Jaeger J, Harris MP, Rowlands DJ, , 2003. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett 535: 3438.[Crossref]
  61. Sanz MA, Madan V, Carrasco L, Nieva JL, , 2003. Interfacial domains in Sindbis virus 6K protein. Detection and functional characterization. J Biol Chem 278: 20512057.[Crossref]
  62. Joubert DA, Blasdell KR, Audsley MD, Trinidad L, Monaghan P, Dave KA, Lieu K, Amos-Ritchie R, Jans DA, Moseley GW, Gorman JJ, Walker PJ, , 2014. Bovine ephemeral fever rhabdovirus α1 protein has viroporin-like properties and binds importin β1 and importin 7. J Virol 88: 15911603.[Crossref]
  63. Hout DR, Mulcahy ER, Pacyniak E, Gomez LM, Gomez ML, Stephens EB, , 2004. VPU: a multifunctional protein that enhances the pathogenesis of human immunodeficiency virus type 1. Curr HIV Res 2: 255270.[Crossref]
  64. Griffin SD, , 2009. Plugging the holes in hepatitis C virus antiviral therapy. Proc Natl Acad Sci USA 106: 1256712568.[Crossref]
  65. Causey OR, Kemp GE, Madbouly MH, David-West TS, , 1970. Congo virus from domestic livestock, African hedgehog, and arthropods in Nigeria. Am J Trop Med Hyg 19: 846850.
  66. Begum F, Wisseman CL, Jr Casals J, , 1970. Tick-borne viruses of west Pakistan. II. Hazara virus, a new agent isolated from Ixodes redikorzevi ticks from the Kaghan Valley, W. Pakistan. Am J Epidemiol 92: 192194.[Crossref]
  67. Dandawate CN, Shah KV, , 1969. Ganjam virus: a new arbovirus isolated from ticks Haemaphysalis intermedia Warburton and Nuttall, 1909 in Orissa, India. Indian J Med Res 57: 799804.
  68. Crabtree MB, Sang R, Miller BR, , 2009. Kupe virus, a new virus in the family Bunyaviridae, genus Nairovirus, Kenya. Emerg Infect Dis 15: 147154.[Crossref]
  69. Ward VK, Marriott AC, el-Ghorr AA, Nuttall PA, , 1990. Coding strategy of the S RNA segment of Dugbe virus (Nairovirus; Bunyaviridae). Virology 175: 518524.[Crossref]
  70. Dacheux L, Cervantes-Gonzalez M, Guigon G, Thiberge JM, Vandenbogaert M, Maufrais C, Caro V, Bourhy H, , 2014. A preliminary study of viral metagenomics of French bat species in contact with humans: identification of new mammalian viruses. PLoS One 9: e87194.[Crossref]
  71. Al'khovskii SV, L'vov DK, Shchelkanov M, Shchetinin AM, Deriabin PG, Gitel'man AK, Botikov AG, Samokhvalov EI, Zakarian VA, , 2014. Taxonomic status of the Artashat virus (ARTSV) (Bunyaviridae, Nairovirus) isolated from the ticks Ornithodoros alactagalis Issaakjan, 1936 and O. verrucosus Olenev, Sassuchin et Fenuk, 1934 (Argasidae Koch, 1844) collected in Transcaucasia [in Russian]. Vopr Virusol 59: 2428.
  72. Chastel C, Main AJ, Richard P, Le Lay G, Legrand-Quillien MC, Beaucournu JC, , 1989. Erve virus, a probable member of Bunyaviridae family isolated from shrews (Crocidura russula) in France. Acta Virol 33: 270280.
  73. Varma MG, Converse JD, , 1976. Keterah virus infections in four species of Argas ticks (Ixodoidea: Argasidae). J Med Entomol 13: 6570.[Crossref]
  74. Al'khovskii SV, L'vov DK, Shchelkanov M, Deriabin PG, Shchetinin AM, Samokhvalov EI, Aristova VA, Gitel'man AK, Botikov AG, , 2014. Genetic characterization of the Uzun-Agach virus (UZAV, Bunyaviridae, Nairovirus), isolated from bat Myotis blythii oxygnathus Monticelli, 1885 (Chiroptera; Vespertilionidae) in Kazakhstan [in Russian]. Vopr Virusol 59: 2326.
  75. Lvov DK, Karas FR, Timofeev EM, Tsyrkin YM, Vargina SG, Veselovskaya OV, Osipova NZ, Grebenyuk YI, Gromashesvki VL, Steblyanko SN, Fomina KB, , 1973. “Issyk-Kul” virus, a new arbovirus isolated from bats and Argas (Carios) vespertilionis (Latr., 1802) in the Kirghiz S.S.R. Arch Gesamte Virusforsch 42: 207209.[Crossref]
  76. Ishii A, Ueno K, Orba Y, Sasaki M, Moonga L, Hang'ombe BM, Mweene AS, Umemura T, Ito K, Hall WW, Sawa H, , 2014. A nairovirus isolated from African bats causes haemorrhagic gastroenteritis and severe hepatic disease in mice. Nat Commun 5: 5651.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.15-0917
Loading
/content/journals/10.4269/ajtmh.15-0917
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

  • Received : 22 Dec 2015
  • Accepted : 13 Jan 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error