Calisher CH, Lazuick JS, Justines G, Francy DB, Monath TP, Gutierrez E, Sabattini MS, Bowen GS, Jakob WL, 1981. Viruses isolated from Aedeomyia squamipennis mosquitoes collected in Panama, Ecuador, and Argentina: establishment of the Gamboa serogroup. Am J Trop Med Hyg 30: 219–223.
Calisher CH, Lazuick JS, Sudia WD, 1988. Brus Laguna virus, a Gamboa bunyavirus from Aedeomyia squamipennis collected in Honduras. Am J Trop Med Hyg 39: 406–408.
Dutary BE, Petersen JL, Peralta PH, Tesh RB, 1989. Transovarial transmission of Gamboa virus in a tropical mosquito, Aedeomyia squamipennis. Am J Trop Med Hyg 40: 108–113.
Degallier N, Travassos da Rosa A, Vasconcelos PF, Herve JP, Sa Filho GC, Travassos Da Rosa JF, Travassos Da Rosa ES, Rodrigues SG, 1992. Modifications of arbovirus transmission in relation to construction of dams in Brazilian Amazonia. Cienc Cult 44: 124–135.
Eastwood G, Loaiza JR, Pongsiri MJ, Sanjur OI, Pecor JE, Auguste AJ, Kramer LD, 2016. Enzootic arbovirus surveillance in forest habitat and phylogenetic characterization of novel isolates of Gamboa virus in Panama. Am J Trop Med Hyg 94: 786–793.
Elliott RM, 2014. Orthobunyaviruses: recent genetic and structural insights. Nat Rev Microbiol 12: 673–685.
Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Muller WE, Wetter T, Suhai S, 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14: 1147–1159.
Krogh A, Larsson B, von Heijne G, Sonnhammer EL, 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567–580.
Petersen TN, Brunak S, von Heijne G, Nielsen H, 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786.
Zuker M, 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415.
Edgar RC, 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ, 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32: 268–274.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725–2729.
Katoh K, Standley DM, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780.
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B, 2015. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1: vev003.
Clarke DH, Casals J, 1958. Techniques for hemagglutination and hemagglutination-inhibition with arthropod-borne viruses. Am J Trop Med Hyg 7: 561–573.
Beaty BJ, Calisher CH, Shope RE, 1989. Diagnostic Procerdures for Viral Rickettsial and Chlamydial Infections. Washington, DC: American Public Health Association.
Quaresma JA, Barros VL, Fernandes ER, Pagliari C, Takakura C, da Costa Vasconcelos PF, de Andrade HF Jr, Duarte MI, 2005. Reconsideration of histopathology and ultrastructural aspects of the human liver in yellow fever. Acta Trop 94: 116–127.
Martins LC, Diniz JA, Silva EV, Barros VL, Monteiro HA, Azevedo RS, Quaresma JA, Vasconcelos PF, 2007. Characterization of Minacu virus (Reoviridae: Orbivirus) and pathological changes in experimentally infected newborn mice. Int J Exp Pathol 88: 63–73.
Quaresma JA, Barros VL, Pagliari C, Fernandes ER, Guedes F, Takakura CF, Andrade HF Jr, Vasconcelos PF, Duarte MI, 2006. Revisiting the liver in human yellow fever: virus-induced apoptosis in hepatocytes associated with TGF-beta, TNF-alpha and NK cells activity. Virology 345: 22–30.
de Souza WM, Acrani GO, Romeiro MF, Reis O Jr, Tolardo AL, da Silva SP, de Almeida Medeiros DB, Varela M, Nunes MR, Figueiredo LT, 2016. Molecular characterization of Capim and Enseada orthobunyaviruses. Infect Genet Evol 40: 47–53.
Shi X, Kohl A, Leonard VH, Li P, McLees A, Elliott RM, 2006. Requirement of the N-terminal region of Orthobunyavirus nonstructural protein NSm for virus assembly and morphogenesis. J Virol 80: 8089–8099.
Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, Ludkvist A, Schmaljohn CS, Tesh RB, 2012. Family Bunyaviridae. King AMQ, Adams EB, Carstens E, Lefkowitz EJ, eds. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. New York, NY: Elsevier Academic Press, 725–741.
Reguera J, Weber F, Cusack S, 2010. Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog 6: e1001101.
Pollitt E, Zhao J, Muscat P, Elliott RM, 2006. Characterization of Maguari Orthobunyavirus mutants suggests the nonstructural protein NSm is not essential for growth in tissue culture. Virology 348: 224–232.
Kraatz F, Wernike K, Hechinger S, Konig P, Granzow H, Reimann I, Beer M, 2015. Deletion mutants of Schmallenberg virus are avirulent and protect from virus challenge. J Virol 89: 1825–1837.
Tilston-Lunel NL, Acrani GO, Randall RE, Elliott RM, 2015. Generation of recombinant Oropouche viruses lacking the nonstructural protein NSm or NSs. J Virol 90: 2616–2627.
Shchetinin AM, Lvov DK, Deriabin PG, Botikov AG, Gitelman AK, Kuhn JH, Alkhovsky SV, 2015. Genetic and phylogenetic characterization of tataguine and Witwatersrand viruses and other orthobunyaviruses of the Anopheles A, Capim, Guama, Koongol, Mapputta, Tete, and Turlock serogroups. Viruses 7: 5987–6008.
Doherty RL, Carley JG, Mackerras MJ, Marks EN, 1963. Studies of arthropod-borne virus infections in Queensland. III. Isolation and characterization of virus strains from wild-caught mosquitoes in north Queensland. Aust J Exp Biol Med Sci 41: 17–39.
Shope RE, Causey OR, 1962. Further studies on the serological relationships of group C arthropod-borne viruses and the application of these relationships to rapid identification of types. Am J Trop Med Hyg 11: 283–290.
Briese T, Calisher CH, Higgs S, 2013. Viruses of the family Bunyaviridae: are all available isolates reassortants? Virology 446: 207–216.
Peters CJ, Zaki SR, 1997. Hantavirus pulmonary syndrome. Horsburgh CR Jr, Nelson AM, eds. Pathology of Emerging Infections. Washington, DC: ASM Press, 95–106.
Jonsson CB, Figueiredo LT, Vapalahti O, 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412–441.
Forattini OP, 2002. Tribo Sabethini. Forattini OP, ed. Culicidologia Medica: Identificacao, Biologia e Epidemiologia. Sao Paulo, Brazil: Edusp, 759–760.
Knight KL, Stone A, 1977. A Catalogue of the Mosquitoes of the World (Diptera: Culicidae). College Park, MD: Entomologic Society of America.
Dutary BE, Petersen JL, Peralta PH, Galindo P, Tesh RB, 1987. Mechanisms for the maintenance of Gamboa virus in the mosquito Aedeomyia squamipennis [in Spanish]. Rev Med Panama 12: 182–188.
Petersen JL, Linley JR, 1995. Description of the egg of Aedeomyia squamipennis (Diptera: Culicidae). J Med Entomol 32: 888–894.
Galindo P, Adames AJ, Peralta PH, Johnson CM, Read R, 1983. Impact of the Bayano hydroelectric project on the transmission of arboviruses [in Spanish]. Rev Med Panama 8: 89–134.
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Comprehensive comparative phylogenetic analyses were performed on 17 Gamboa serogroup viruses (GAMSVs) from distinct geographic regions in the Americas and other representative members of the genus Orthobunyavirus (Peribunyaviridae), based on small (S), medium (M), and large (L) open reading frame full-length and partial sequences. Genome characterization showed that the GAMSVs divide into four clades or genotypes. The GAMSVs have a genetic organization similar to other orthobunyaviruses, except that they have a larger NSm protein than other orthobunyaviruses. A serosurvey for Gamboa virus antibodies was performed in plasma from birds, other wild animals, and humans living around the Tucuruí hydroelectric dam in Pará state, northern Brazil, a known focus of GAMSV activity. Newborn chicks (Gallus gallus domesticus) were experimentally infected with a GAMSV, and the pathogenesis is described. Histopathological changes were primarily in the lungs and liver. Also, a review of the ecology of the GAMSVs in the Americas is included. In sum, this study presents the genomic and evolutionary characterization of the Gamboa group and the potential model of pathogenesis, which would be helpful for diagnostic purposes, epidemiology, and immunopathogenesis studies.
These authors contributed equally to this work.
Deceased.
Financial support: Work in Brazil was partially supported by CNPq grants 302987/2008-8, 302584/2015-3 (MRTN), 303999/2016-0, and 457664/2013-4 (PICV), CAPES (JOC), and the Instituto Evandro Chagas/Brazilian Ministry of Health. W.M.d.S. was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil (Scholarships No. 12/24150-9 and 15/05778-5). Work in Panama was supported in part by grants AI02984, AI11889, and AI22122 from the U.S. National Institutes of Health (NIH). Work in the United States was supported by NIH grant 1R24 AI120942 and contract HHSN272201000040I/HHSN27200004/D04.
Authors’ addresses: Jannifer Oliveira Chiang, Márcio Roberto Teixeira Nunes, Sandro Patroca da Silva, Pedro Henrique Dorta de Silva, Alana Watanabe de Sousa, Sueli Guerreiro Rodrigues, and Pedro Fernando da Costa Vasconcelos, Instituto Evandro Chagas/SVS/MS, Ananindeua, Brazil, E-mails: janniferchiang@iec.pa.gov.br, marcionunesbrasil@yahoo.com.br, spatroca@gmail.com, p_hdorta@yahoo.com.br, alanasousa@iec.pa.gov.br, suelirodrigues.sgr@gmail.com, and pedrovasconcelos@iec.pa.gov.br. William Marciel de Souza, Centro de Pesquisa em Virologia, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil, E-mail: wmarciel@hotmail.com. Gustavo Olszanski Acrani, Universidade Federal da Fronteira Sul, Passo Fundo, Brazil, E-mail: gacrani@gmail.com. Amélia Paes de Andrade Travassos da Rosa, Hilda Guzmán, Nikos Vasilakis, and Robert B. Tesh, University of Texas Medical Branch, Galveston, TX, E-mails: aptravas@gmail.com, hguzman@utmb.edu, nivasila@utmb.edu, and rbtesh22@gmail.com. Nelma Mesquita de Freitas, Centro de Educação Profissional Graziela Reis de Souza, Macapá, Brazil, E-mail: projetos@lacen.ap.gov.br. Juarez Antônio Simões Quaresma, Universidade Federal do Pará, Belém, Brazil, E-mail: juarez.quaresma@gmail.com. Bedsy Dutary, Gorgas Memorial Institute of Health Studies, E-mail: casa.thatcher@gmail.com.
Calisher CH, Lazuick JS, Justines G, Francy DB, Monath TP, Gutierrez E, Sabattini MS, Bowen GS, Jakob WL, 1981. Viruses isolated from Aedeomyia squamipennis mosquitoes collected in Panama, Ecuador, and Argentina: establishment of the Gamboa serogroup. Am J Trop Med Hyg 30: 219–223.
Calisher CH, Lazuick JS, Sudia WD, 1988. Brus Laguna virus, a Gamboa bunyavirus from Aedeomyia squamipennis collected in Honduras. Am J Trop Med Hyg 39: 406–408.
Dutary BE, Petersen JL, Peralta PH, Tesh RB, 1989. Transovarial transmission of Gamboa virus in a tropical mosquito, Aedeomyia squamipennis. Am J Trop Med Hyg 40: 108–113.
Degallier N, Travassos da Rosa A, Vasconcelos PF, Herve JP, Sa Filho GC, Travassos Da Rosa JF, Travassos Da Rosa ES, Rodrigues SG, 1992. Modifications of arbovirus transmission in relation to construction of dams in Brazilian Amazonia. Cienc Cult 44: 124–135.
Eastwood G, Loaiza JR, Pongsiri MJ, Sanjur OI, Pecor JE, Auguste AJ, Kramer LD, 2016. Enzootic arbovirus surveillance in forest habitat and phylogenetic characterization of novel isolates of Gamboa virus in Panama. Am J Trop Med Hyg 94: 786–793.
Elliott RM, 2014. Orthobunyaviruses: recent genetic and structural insights. Nat Rev Microbiol 12: 673–685.
Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Muller WE, Wetter T, Suhai S, 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14: 1147–1159.
Krogh A, Larsson B, von Heijne G, Sonnhammer EL, 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567–580.
Petersen TN, Brunak S, von Heijne G, Nielsen H, 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786.
Zuker M, 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415.
Edgar RC, 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ, 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32: 268–274.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725–2729.
Katoh K, Standley DM, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780.
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B, 2015. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1: vev003.
Clarke DH, Casals J, 1958. Techniques for hemagglutination and hemagglutination-inhibition with arthropod-borne viruses. Am J Trop Med Hyg 7: 561–573.
Beaty BJ, Calisher CH, Shope RE, 1989. Diagnostic Procerdures for Viral Rickettsial and Chlamydial Infections. Washington, DC: American Public Health Association.
Quaresma JA, Barros VL, Fernandes ER, Pagliari C, Takakura C, da Costa Vasconcelos PF, de Andrade HF Jr, Duarte MI, 2005. Reconsideration of histopathology and ultrastructural aspects of the human liver in yellow fever. Acta Trop 94: 116–127.
Martins LC, Diniz JA, Silva EV, Barros VL, Monteiro HA, Azevedo RS, Quaresma JA, Vasconcelos PF, 2007. Characterization of Minacu virus (Reoviridae: Orbivirus) and pathological changes in experimentally infected newborn mice. Int J Exp Pathol 88: 63–73.
Quaresma JA, Barros VL, Pagliari C, Fernandes ER, Guedes F, Takakura CF, Andrade HF Jr, Vasconcelos PF, Duarte MI, 2006. Revisiting the liver in human yellow fever: virus-induced apoptosis in hepatocytes associated with TGF-beta, TNF-alpha and NK cells activity. Virology 345: 22–30.
de Souza WM, Acrani GO, Romeiro MF, Reis O Jr, Tolardo AL, da Silva SP, de Almeida Medeiros DB, Varela M, Nunes MR, Figueiredo LT, 2016. Molecular characterization of Capim and Enseada orthobunyaviruses. Infect Genet Evol 40: 47–53.
Shi X, Kohl A, Leonard VH, Li P, McLees A, Elliott RM, 2006. Requirement of the N-terminal region of Orthobunyavirus nonstructural protein NSm for virus assembly and morphogenesis. J Virol 80: 8089–8099.
Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, Ludkvist A, Schmaljohn CS, Tesh RB, 2012. Family Bunyaviridae. King AMQ, Adams EB, Carstens E, Lefkowitz EJ, eds. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. New York, NY: Elsevier Academic Press, 725–741.
Reguera J, Weber F, Cusack S, 2010. Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog 6: e1001101.
Pollitt E, Zhao J, Muscat P, Elliott RM, 2006. Characterization of Maguari Orthobunyavirus mutants suggests the nonstructural protein NSm is not essential for growth in tissue culture. Virology 348: 224–232.
Kraatz F, Wernike K, Hechinger S, Konig P, Granzow H, Reimann I, Beer M, 2015. Deletion mutants of Schmallenberg virus are avirulent and protect from virus challenge. J Virol 89: 1825–1837.
Tilston-Lunel NL, Acrani GO, Randall RE, Elliott RM, 2015. Generation of recombinant Oropouche viruses lacking the nonstructural protein NSm or NSs. J Virol 90: 2616–2627.
Shchetinin AM, Lvov DK, Deriabin PG, Botikov AG, Gitelman AK, Kuhn JH, Alkhovsky SV, 2015. Genetic and phylogenetic characterization of tataguine and Witwatersrand viruses and other orthobunyaviruses of the Anopheles A, Capim, Guama, Koongol, Mapputta, Tete, and Turlock serogroups. Viruses 7: 5987–6008.
Doherty RL, Carley JG, Mackerras MJ, Marks EN, 1963. Studies of arthropod-borne virus infections in Queensland. III. Isolation and characterization of virus strains from wild-caught mosquitoes in north Queensland. Aust J Exp Biol Med Sci 41: 17–39.
Shope RE, Causey OR, 1962. Further studies on the serological relationships of group C arthropod-borne viruses and the application of these relationships to rapid identification of types. Am J Trop Med Hyg 11: 283–290.
Briese T, Calisher CH, Higgs S, 2013. Viruses of the family Bunyaviridae: are all available isolates reassortants? Virology 446: 207–216.
Peters CJ, Zaki SR, 1997. Hantavirus pulmonary syndrome. Horsburgh CR Jr, Nelson AM, eds. Pathology of Emerging Infections. Washington, DC: ASM Press, 95–106.
Jonsson CB, Figueiredo LT, Vapalahti O, 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412–441.
Forattini OP, 2002. Tribo Sabethini. Forattini OP, ed. Culicidologia Medica: Identificacao, Biologia e Epidemiologia. Sao Paulo, Brazil: Edusp, 759–760.
Knight KL, Stone A, 1977. A Catalogue of the Mosquitoes of the World (Diptera: Culicidae). College Park, MD: Entomologic Society of America.
Dutary BE, Petersen JL, Peralta PH, Galindo P, Tesh RB, 1987. Mechanisms for the maintenance of Gamboa virus in the mosquito Aedeomyia squamipennis [in Spanish]. Rev Med Panama 12: 182–188.
Petersen JL, Linley JR, 1995. Description of the egg of Aedeomyia squamipennis (Diptera: Culicidae). J Med Entomol 32: 888–894.
Galindo P, Adames AJ, Peralta PH, Johnson CM, Read R, 1983. Impact of the Bayano hydroelectric project on the transmission of arboviruses [in Spanish]. Rev Med Panama 8: 89–134.
Past two years | Past Year | Past 30 Days | |
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Abstract Views | 34 | 34 | 17 |
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