Skip to main content
Top
Published in: Virology Journal 1/2013

Open Access 01-12-2013 | Research

Comparative full length genome sequence analysis of usutu virus isolates from Africa

Authors: Birgit Nikolay, Anne Dupressoir, Cadhla Firth, Ousmane Faye, Cheikh S Boye, Mawlouth Diallo, Amadou A Sall

Published in: Virology Journal | Issue 1/2013

Login to get access

Abstract

Background

Usutu virus (USUV), a flavivirus belonging to the Japanese encephalitis serocomplex, was identified in South Africa in 1959 and reported for the first time in Europe in 2001. To date, full length genome sequences have been available only for the reference strain from South Africa and a single isolate from each of Austria, Hungary, and Italy.

Methods

We sequenced four USUV isolates from Senegal and the Central African Republic (CAR) between 1974 and 2007 and compared the sequence data to USUV strains from Austria, Hungary, Italy, and South Africa using a Bayesian Markov chain Monte Carlo method. We further clarified the taxonomic status of a USUV strain isolated in CAR in 1969 and proposed earlier as a subtype of USUV due to an asymetric serological cross-reactivity with USUV reference strain.

Results

A comparison of the four newly obtained USUV sequences with those from SouthAfrica_1959, Vienna_2001, Budapest_2005, and Italy_2009 revealed that they are all 96-99% and 99% similar at the nucleotide and amino acid levels, respectively. The phylogenetic relationships between these sequences indicated that a strain isolated in Senegal in 1993 is most closely related to the USUV strains detected in Europe. Analysis of a strain isolated from a human in CAR in 1981 (CAR_1981) revealed the presence of specific amino acid substitutions and a deletion in the 3′ noncoding region. This is the first fully sequenced human USUV isolate.
The putative USUV subtype, CAR_1969, was 81% and 94% identical at the nucleotide and amino acid levels, respectively, compared to the other USUV strains. Our phylogenetic analyses support the serological identification of CAR_1969 as a subtype of USUV.

Conclusions

In this study, we investigate the genetic diversity of USUV in Africa and the phylogenetic relationship of isolates from Africa and Europe for the first time. The results suggest a low genetic diversity within USUV, the existence of a distinct USUV subtype strain, and support the hypothesis that USUV was introduced to Europe from Africa. Further sequencing and analysis of USUV isolates from other African countries would contribute to a better understanding of its genetic diversity and geographic distribution.
Appendix
Available only for authorised users
Literature
1.
go back to reference Woodall JP: The viruses isolated from arthropods at the East African Virus Research Institute in the 26 years ending December 1963. Proc E Afrc Acad. 1964, II: 141-146. Woodall JP: The viruses isolated from arthropods at the East African Virus Research Institute in the 26 years ending December 1963. Proc E Afrc Acad. 1964, II: 141-146.
2.
go back to reference Poidinger M, Hall RA, Mackenzie JS: Molecular characterization of the Japanese encephalitis serocomplex of the flavivirus genus. Virology. 1996, 218 (2): 417-421. 10.1006/viro.1996.0213.PubMedCrossRef Poidinger M, Hall RA, Mackenzie JS: Molecular characterization of the Japanese encephalitis serocomplex of the flavivirus genus. Virology. 1996, 218 (2): 417-421. 10.1006/viro.1996.0213.PubMedCrossRef
3.
go back to reference Nikolay B, Diallo M, Boye CS, Sall AA: Usutu Virus in Africa. Vector Borne Zoonotic Dis. 2011, 11 (11): 1417-1423. 10.1089/vbz.2011.0631.PubMedCrossRef Nikolay B, Diallo M, Boye CS, Sall AA: Usutu Virus in Africa. Vector Borne Zoonotic Dis. 2011, 11 (11): 1417-1423. 10.1089/vbz.2011.0631.PubMedCrossRef
4.
go back to reference Weissenbock H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N: Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis. 2002, 8 (7): 652-656. 10.3201/eid0807.020094.PubMedPubMedCentralCrossRef Weissenbock H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N: Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis. 2002, 8 (7): 652-656. 10.3201/eid0807.020094.PubMedPubMedCentralCrossRef
5.
6.
go back to reference Weissenbock H, Kolodziejek J, Fragner K, Kuhn R, Pfeffer M, Nowotny N: Usutu virus activity in Austria, 2001–2002. Microbes Infect. 2003, 5 (12): 1132-1136. 10.1016/S1286-4579(03)00204-1.PubMedCrossRef Weissenbock H, Kolodziejek J, Fragner K, Kuhn R, Pfeffer M, Nowotny N: Usutu virus activity in Austria, 2001–2002. Microbes Infect. 2003, 5 (12): 1132-1136. 10.1016/S1286-4579(03)00204-1.PubMedCrossRef
7.
go back to reference Nikolay B, Diallo M, Faye O, Boye CS, Sall AA: Vector competence of Cx. neavei (Diptera: Culicidae) for Usutu virus. AmJTrop Med Hyg. 2012, 86 (6): 993-996. 10.4269/ajtmh.2012.11-0509.CrossRef Nikolay B, Diallo M, Faye O, Boye CS, Sall AA: Vector competence of Cx. neavei (Diptera: Culicidae) for Usutu virus. AmJTrop Med Hyg. 2012, 86 (6): 993-996. 10.4269/ajtmh.2012.11-0509.CrossRef
8.
go back to reference Bakonyi T, Erdelyi K, Ursu K, Ferenczi E, Csorgo T, Lussy H, Chvala S, Bukovsky C, Meister T, Weissenbock H, et al: Emergence of Usutu virus in Hungary. J Clin Microbiol. 2007, 45 (12): 3870-3874. 10.1128/JCM.01390-07.PubMedPubMedCentralCrossRef Bakonyi T, Erdelyi K, Ursu K, Ferenczi E, Csorgo T, Lussy H, Chvala S, Bukovsky C, Meister T, Weissenbock H, et al: Emergence of Usutu virus in Hungary. J Clin Microbiol. 2007, 45 (12): 3870-3874. 10.1128/JCM.01390-07.PubMedPubMedCentralCrossRef
9.
go back to reference Buckley A, Dawson A, Moss SR, Hinsley SA, Bellamy PE, Gould EA: Serological evidence of West Nile virus, Usutu virus and Sindbis virus infection of birds in the UK. J Gen Virol. 2003, 84 (Pt 10): 2807-2817.PubMedCrossRef Buckley A, Dawson A, Moss SR, Hinsley SA, Bellamy PE, Gould EA: Serological evidence of West Nile virus, Usutu virus and Sindbis virus infection of birds in the UK. J Gen Virol. 2003, 84 (Pt 10): 2807-2817.PubMedCrossRef
10.
go back to reference Busquets N, Alba A, Allepuz A, Aranda C, Ignacio Nunez J: Usutu virus sequences in Culex pipiens (Diptera: Culicidae), Spain. Emerg Infect Dis. 2008, 14 (5): 861-863. 10.3201/eid1405.071577.PubMedPubMedCentralCrossRef Busquets N, Alba A, Allepuz A, Aranda C, Ignacio Nunez J: Usutu virus sequences in Culex pipiens (Diptera: Culicidae), Spain. Emerg Infect Dis. 2008, 14 (5): 861-863. 10.3201/eid1405.071577.PubMedPubMedCentralCrossRef
11.
go back to reference Hubalek Z, Halouzka J, Juricova Z, Sikutova S, Rudolf I, Honza M, Jankova J, Chytil J, Marec F, Sitko J: Serologic survey of birds for West Nile flavivirus in southern Moravia (Czech Republic). Vector Borne Zoonotic Dis. 2008, 8 (5): 659-666. 10.1089/vbz.2007.0283.PubMedCrossRef Hubalek Z, Halouzka J, Juricova Z, Sikutova S, Rudolf I, Honza M, Jankova J, Chytil J, Marec F, Sitko J: Serologic survey of birds for West Nile flavivirus in southern Moravia (Czech Republic). Vector Borne Zoonotic Dis. 2008, 8 (5): 659-666. 10.1089/vbz.2007.0283.PubMedCrossRef
12.
go back to reference Hubalek Z, Wegner E, Halouzka J, Tryjanowski P, Jerzak L, Sikutova S, Rudolf I, Kruszewicz AG, Jaworski Z, Wlodarczyk R: Serologic survey of potential vertebrate hosts for West Nile virus in Poland. Viral Immunol. 2008, 21 (2): 247-253. 10.1089/vim.2007.0111.PubMedCrossRef Hubalek Z, Wegner E, Halouzka J, Tryjanowski P, Jerzak L, Sikutova S, Rudolf I, Kruszewicz AG, Jaworski Z, Wlodarczyk R: Serologic survey of potential vertebrate hosts for West Nile virus in Poland. Viral Immunol. 2008, 21 (2): 247-253. 10.1089/vim.2007.0111.PubMedCrossRef
13.
go back to reference Lelli R, Savini G, Teodori L, Filipponi G, Di Gennaro A, Leone A, Di Gialleonardo L, Venturi L, Caporale V: Serological evidence of Usutu virus occurrence in north-eastern Italy. Zoonoses Public Health. 2008, 55 (7): 361-367. 10.1111/j.1863-2378.2008.01146.x.PubMedCrossRef Lelli R, Savini G, Teodori L, Filipponi G, Di Gennaro A, Leone A, Di Gialleonardo L, Venturi L, Caporale V: Serological evidence of Usutu virus occurrence in north-eastern Italy. Zoonoses Public Health. 2008, 55 (7): 361-367. 10.1111/j.1863-2378.2008.01146.x.PubMedCrossRef
14.
go back to reference Linke S, Niedrig M, Kaiser A, Ellerbrok H, Muller K, Muller T, Conraths FJ, Muhle RU, Schmidt D, Koppen U, et al: Serologic evidence of West Nile virus infections in wild birds captured in Germany. AmJTrop Med Hyg. 2007, 77 (2): 358-364. Linke S, Niedrig M, Kaiser A, Ellerbrok H, Muller K, Muller T, Conraths FJ, Muhle RU, Schmidt D, Koppen U, et al: Serologic evidence of West Nile virus infections in wild birds captured in Germany. AmJTrop Med Hyg. 2007, 77 (2): 358-364.
15.
go back to reference Steinmetz HW, Bakonyi T, Weissenbock H, Hatt JM, Eulenberger U, Robert N, Hoop R, Nowotny N: Emergence and establishment of Usutu virus infection in wild and captive avian species in and around Zurich, Switzerland-Genomic and pathologic comparison to other central European outbreaks. Vet Microbiol. 2011, 148 (2–4): 207-212.PubMedCrossRef Steinmetz HW, Bakonyi T, Weissenbock H, Hatt JM, Eulenberger U, Robert N, Hoop R, Nowotny N: Emergence and establishment of Usutu virus infection in wild and captive avian species in and around Zurich, Switzerland-Genomic and pathologic comparison to other central European outbreaks. Vet Microbiol. 2011, 148 (2–4): 207-212.PubMedCrossRef
16.
go back to reference Cavrini F, Gaibani P, Longo G, Pierro AM, Rossini G, Bonilauri P, Gerundi GE, Di Benedetto F, Pasetto A, Girardis M, et al: Usutu virus infection in a patient who underwent orthotropic liver transplantation, Italy, August-September 2009. Euro Surveill. 2009, 14 (50): pii=19448- Cavrini F, Gaibani P, Longo G, Pierro AM, Rossini G, Bonilauri P, Gerundi GE, Di Benedetto F, Pasetto A, Girardis M, et al: Usutu virus infection in a patient who underwent orthotropic liver transplantation, Italy, August-September 2009. Euro Surveill. 2009, 14 (50): pii=19448-
17.
go back to reference Pecorari M, Longo G, Gennari W, Grottola A, Sabbatini A, Tagliazucchi S, Savini G, Monaco F, Simone M, Lelli R, et al: First human case of Usutu virus neuroinvasive infection, Italy, August-September 2009. Euro Surveill. 2009, 14 (50): pii=19446- Pecorari M, Longo G, Gennari W, Grottola A, Sabbatini A, Tagliazucchi S, Savini G, Monaco F, Simone M, Lelli R, et al: First human case of Usutu virus neuroinvasive infection, Italy, August-September 2009. Euro Surveill. 2009, 14 (50): pii=19446-
18.
go back to reference Bakonyi T, Gould EA, Kolodziejek J, Weissenbock H, Nowotny N: Complete genome analysis and molecular characterization of Usutu virus that emerged in Austria in 2001: comparison with the South African strain SAAR-1776 and other flaviviruses. Virology. 2004, 328 (2): 301-310.PubMed Bakonyi T, Gould EA, Kolodziejek J, Weissenbock H, Nowotny N: Complete genome analysis and molecular characterization of Usutu virus that emerged in Austria in 2001: comparison with the South African strain SAAR-1776 and other flaviviruses. Virology. 2004, 328 (2): 301-310.PubMed
19.
go back to reference Hurrelbrink RJ, McMinn PC: Molecular determinants of virulence: the structural and functional basis for flavivirus attenuation. Adv Virus Res. 2003, 60: 1-42.PubMedCrossRef Hurrelbrink RJ, McMinn PC: Molecular determinants of virulence: the structural and functional basis for flavivirus attenuation. Adv Virus Res. 2003, 60: 1-42.PubMedCrossRef
20.
go back to reference Cook S, Holmes EC: A multigene analysis of the phylogenetic relationships among the flaviviruses (Family: Flaviviridae) and the evolution of vector transmission. Arch Virol. 2006, 151 (2): 309-325. 10.1007/s00705-005-0626-6.PubMedCrossRef Cook S, Holmes EC: A multigene analysis of the phylogenetic relationships among the flaviviruses (Family: Flaviviridae) and the evolution of vector transmission. Arch Virol. 2006, 151 (2): 309-325. 10.1007/s00705-005-0626-6.PubMedCrossRef
21.
go back to reference Kuno G, Chang GJ, Tsuchiya KR, Karabatsos N, Cropp CB: Phylogeny of the genus Flavivirus. J Virol. 1998, 72 (1): 73-83.PubMedPubMedCentral Kuno G, Chang GJ, Tsuchiya KR, Karabatsos N, Cropp CB: Phylogeny of the genus Flavivirus. J Virol. 1998, 72 (1): 73-83.PubMedPubMedCentral
22.
go back to reference Savini G, Monaco F, Terregino C, Di Gennaro A, Bano L, Pinoni C, De Nardi R, Bonilauri P, Pecorari M, Di Gialleonardo L, et al: Usutu virus in ITALY: An emergence or a silent infection?. Vet Microbiol. 2011, 151 (3–4): 264-274.PubMedCrossRef Savini G, Monaco F, Terregino C, Di Gennaro A, Bano L, Pinoni C, De Nardi R, Bonilauri P, Pecorari M, Di Gialleonardo L, et al: Usutu virus in ITALY: An emergence or a silent infection?. Vet Microbiol. 2011, 151 (3–4): 264-274.PubMedCrossRef
23.
go back to reference Institut Pasteur de Dakar: Rapport annuel. 1970 Institut Pasteur de Dakar: Rapport annuel. 1970
24.
go back to reference Woelk CH, Holmes EC: Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol. 2002, 19 (12): 2333-2336. 10.1093/oxfordjournals.molbev.a004059.PubMedCrossRef Woelk CH, Holmes EC: Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol. 2002, 19 (12): 2333-2336. 10.1093/oxfordjournals.molbev.a004059.PubMedCrossRef
25.
go back to reference Sall AA, Faye O, Diallo M, Firth C, Kitchen A, Holmes EC: Yellow fever virus exhibits slower evolutionary dynamics than dengue virus. J Virol. 2011, 84 (2): 765-772.CrossRef Sall AA, Faye O, Diallo M, Firth C, Kitchen A, Holmes EC: Yellow fever virus exhibits slower evolutionary dynamics than dengue virus. J Virol. 2011, 84 (2): 765-772.CrossRef
26.
go back to reference Chevalier V, Reynaud P, Lefrancois T, Durand B, Baillon F, Balanca G, Gaidet N, Mondet B, Lancelot R: Predicting West Nile virus seroprevalence in wild birds in Senegal. Vector Borne Zoonotic Dis. 2009, 9 (6): 589-596. 10.1089/vbz.2008.0130.PubMedCrossRef Chevalier V, Reynaud P, Lefrancois T, Durand B, Baillon F, Balanca G, Gaidet N, Mondet B, Lancelot R: Predicting West Nile virus seroprevalence in wild birds in Senegal. Vector Borne Zoonotic Dis. 2009, 9 (6): 589-596. 10.1089/vbz.2008.0130.PubMedCrossRef
27.
go back to reference Institut Pasteur de Dakar: Rapport sur le fonctionnement technique de l’Institut Pasteur de Dakar. 1984, Dakar: Institut Pasteur de Dakar, 1982-1984. Institut Pasteur de Dakar: Rapport sur le fonctionnement technique de l’Institut Pasteur de Dakar. 1984, Dakar: Institut Pasteur de Dakar, 1982-1984.
28.
go back to reference Digoutte JP, Calvo-Wilson MA, Mondo M, Traore-Lamizana M, Adam F: Continuous cell lines and immune ascitic fluid pools in arbovirus detection. Res Virol. 1992, 143 (6): 417-422.PubMedCrossRef Digoutte JP, Calvo-Wilson MA, Mondo M, Traore-Lamizana M, Adam F: Continuous cell lines and immune ascitic fluid pools in arbovirus detection. Res Virol. 1992, 143 (6): 417-422.PubMedCrossRef
29.
go back to reference Crochu S, Cook S, Attoui H, Charrel RN, De Chesse R, Belhouchet M, Lemasson JJ, de Micco P, de Lamballerie X: Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J Gen Virol. 2004, 85 (Pt 7): 1971-1980.PubMedCrossRef Crochu S, Cook S, Attoui H, Charrel RN, De Chesse R, Belhouchet M, Lemasson JJ, de Micco P, de Lamballerie X: Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J Gen Virol. 2004, 85 (Pt 7): 1971-1980.PubMedCrossRef
30.
go back to reference Gaunt MW, Sall AA, de Lamballerie X, Falconar AK, Dzhivanian TI, Gould EA: Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. J Gen Virol. 2001, 82 (Pt 8): 1867-1876.PubMedCrossRef Gaunt MW, Sall AA, de Lamballerie X, Falconar AK, Dzhivanian TI, Gould EA: Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. J Gen Virol. 2001, 82 (Pt 8): 1867-1876.PubMedCrossRef
31.
go back to reference Pierre V, Drouet MT, Deubel V: Identification of mosquito-borne flavivirus sequences using universal primers and reverse transcription/polymerase chain reaction. Res Virol. 1994, 145 (2): 93-104.PubMedCrossRef Pierre V, Drouet MT, Deubel V: Identification of mosquito-borne flavivirus sequences using universal primers and reverse transcription/polymerase chain reaction. Res Virol. 1994, 145 (2): 93-104.PubMedCrossRef
33.
go back to reference Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al: Clustal W and Clustal X version 2.0. Bioinformatics. 2007, 23 (21): 2947-2948. 10.1093/bioinformatics/btm404.PubMedCrossRef Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al: Clustal W and Clustal X version 2.0. Bioinformatics. 2007, 23 (21): 2947-2948. 10.1093/bioinformatics/btm404.PubMedCrossRef
34.
go back to reference Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC: Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol. 1999, 73 (1): 152-160.PubMedPubMedCentral Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC: Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol. 1999, 73 (1): 152-160.PubMedPubMedCentral
35.
go back to reference Pond SL, Frost SD: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005, 21 (10): 2531-2533. 10.1093/bioinformatics/bti320.PubMedCrossRef Pond SL, Frost SD: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005, 21 (10): 2531-2533. 10.1093/bioinformatics/bti320.PubMedCrossRef
36.
go back to reference Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998, 14 (9): 817-818. 10.1093/bioinformatics/14.9.817.PubMedCrossRef Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998, 14 (9): 817-818. 10.1093/bioinformatics/14.9.817.PubMedCrossRef
37.
go back to reference Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). 2003, Sunderland, Massachusetts: Sinauer Associates, 4 Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). 2003, Sunderland, Massachusetts: Sinauer Associates, 4
Metadata
Title
Comparative full length genome sequence analysis of usutu virus isolates from Africa
Authors
Birgit Nikolay
Anne Dupressoir
Cadhla Firth
Ousmane Faye
Cheikh S Boye
Mawlouth Diallo
Amadou A Sall
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2013
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-10-217

Other articles of this Issue 1/2013

Virology Journal 1/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.