Genetic Characteristics and Phylogeographic Dynamics of Echovirus.
Amino acid variation
Echovirus
Genomic recombination
Phylogenetic analysis
Phylogeographic analysis
Journal
Journal of microbiology (Seoul, Korea)
ISSN: 1976-3794
Titre abrégé: J Microbiol
Pays: Korea (South)
ID NLM: 9703165
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
received:
16
06
2023
accepted:
22
08
2023
revised:
20
08
2023
medline:
26
10
2023
pubmed:
15
9
2023
entrez:
15
9
2023
Statut:
ppublish
Résumé
Echoviruses belong to the genus Enterovirus in the Picornaviridae family, forming a large group of Enterovirus B (EV-B) within the Enteroviruses. Previously, Echoviruses were classified based on the coding sequence of VP1. In this study, we performed a reliable phylogenetic classification of 277 sequences isolated from 1992 to 2019 based on the full-length genomes of Echovirus. In this report, phylogenetic, phylogeographic, recombination, and amino acid variability landscape analyses were performed to reveal the evolutional characteristics of Echovirus worldwide. Echoviruses were clustered into nine major clades, e.g., G1-G9. Phylogeographic analysis showed that branches G2-G9 were linked to common strains, while the branch G1 was only linked to G5. In contrast, strains E12, E14, and E16 clustered separately from their G3 and G7 clades respectively, and became a separate branch. In addition, we identified a total of 93 recombination events, where most of the events occurred within the VP1-VP4 coding regions. Analysis of amino acid variation showed high variability in the a positions of VP2, VP1, and VP3. This study updates the phylogenetic and phylogeographic information of Echovirus and indicates that extensive recombination and significant amino acid variation in the capsid proteins drove the emergence of new strains.
Identifiants
pubmed: 37713068
doi: 10.1007/s12275-023-00078-w
pii: 10.1007/s12275-023-00078-w
doi:
Substances chimiques
Capsid Proteins
0
Amino Acids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
865-877Subventions
Organisme : Four batches innovation project of invigorating medical through science and technology of Shanxi province
ID : 2023XM015
Organisme : the Fundamental Research Program of Shanxi Province, China
ID : 20210302124187
Organisme : The Programme of Introducing Talents of Discipline to Universities
ID : D21004
Informations de copyright
© 2023. The Author(s), under exclusive licence to Microbiological Society of Korea.
Références
Abzug, M. J. (2004). Presentation, diagnosis, and management of enterovirus infections in neonates. Pediatric Drugs, 6, 1–10.
pubmed: 14969566
doi: 10.2165/00148581-200406010-00001
Angez, M., Shaukat, S., Zahra, R., Sharif, S., Alam, M. M., Khurshid, A., Rana, M. S., & Zaidi, S. S. (2015). Identification of new genotype of Echovirus 19 from children with Acute Flaccid Paralysis in Pakistan. Scientific Reports, 5, 17456.
pubmed: 26644348
pmcid: 4672337
doi: 10.1038/srep17456
Benschop, K. S. M., Broberg, E. K., Hodcroft, E., Schmitz, D., Albert, J., Baicus, A., Bailly, J. L., Baldvinsdottir, G., Berginc, N., Blomqvist, S., Böttcher, S., Brytting, M., Bujaki, E., Cabrerizo, M., Celma, C., Cinek, O., Claas, E. C. J., Cremer, J., Dean, J., … Demchyshyna, I. (2021). Molecular epidemiology and evolutionary trajectory of emerging Echovirus 30, Europe. Emerging Infectious Diseases, 27, 1616–1626.
pubmed: 34013874
pmcid: 8153861
doi: 10.3201/eid2706.203096
Brouwer, L., Moreni, G., Wolthers, K. C., & Pajkrt, D. (2021). World-wide prevalence and genotype distribution of Enteroviruses. Viruses, 13, 434.
pubmed: 33800518
pmcid: 7999254
doi: 10.3390/v13030434
Castro, C. M., Oliveira, D. S., Macedo, O., Lima, M. J., Santana, M. B., Wanzeller, A. L., Silveira, E., & Gomes, M. L. (2009). Echovirus 30 associated with cases of aseptic meningitis in state of Pará, Northern Brazil. Memorias Do Instituto Oswaldo Cruz, 104, 444–450.
pubmed: 19547870
doi: 10.1590/S0074-02762009000300008
Chen, J. H., Chiu, N. C., Chang, J. H., Huang, F. Y., Wu, K. B., & Lin, T. L. (2005). A neonatal echovirus 11 outbreak in an obstetric clinic. Journal of Microbiology, Immunology, and Infection, 38, 332–337.
pubmed: 16211141
Chen, P., Li, Y., Tao, Z., Wang, H., Lin, X., Liu, Y., Wang, S., Zhou, N., Wang, P., & Xu, A. (2017a). Evolutionary phylogeography and transmission pattern of echovirus 14: An exploration of spatiotemporal dynamics based on the 26-year acute flaccid paralysis surveillance in Shandong, China. BMC Genomics, 18, 48.
pubmed: 28061751
pmcid: 5219651
doi: 10.1186/s12864-016-3418-3
Chen, X., Li, J., Guo, J., Xu, W., Sun, S., & Xie, Z. (2017b). An outbreak of echovirus 18 encephalitis/meningitis in children in Hebei Province, China, 2015. Emerging Microbes & Infections, 6, e54.
doi: 10.1038/emi.2017.39
Chen, X., Qu, X., Liu, C., Zhang, Y., Zhang, G., Han, P., Duan, Y., Li, Q., Wang, L., Ruan, W., Wang, P., Wei, W., Gao, G. F., Zhao, X., & Xie, Z. (2022). Human FcRn is a two-in-one attachment-uncoating receptor for Echovirus 18. mBio, 13, e0116622.
pubmed: 35862785
doi: 10.1128/mbio.01166-22
Diedrich, S., & Schreier, E. (2001). Aseptic meningitis in Germany associated with echovirus type 13. BMC Infectious Diseases, 1, 14.
pubmed: 11591222
pmcid: 57743
doi: 10.1186/1471-2334-1-14
Dilcher, M., Howard, J. C., Dalton, S. C., Anderson, T., Clinghan, R. T., & Werno, A. M. (2022). Clinical, laboratory, and molecular epidemiology of an outbreak of aseptic meningitis due to a triple-recombinant Echovirus in Ashburton, New Zealand. Viruses, 14, 658.
pubmed: 35458388
pmcid: 9030895
doi: 10.3390/v14040658
Faleye, T. O. C., Adewumi, O. M., Klapsa, D., Majumdar, M., Martin, J., & Adeniji, J. A. (2019). Genome Sequences of two dual-serotype-specific Echovirus 20 Strains from Nigeria. Microbiology Resource Announcements, 8, e00894-e919.
pubmed: 31649074
pmcid: 6813386
doi: 10.1128/MRA.00894-19
Fields, B. N., Knipe, D. M., & Howley, P. M. (2007). Fields virology (5th ed.). Wolters Kluwer Health/Lippincott Williams & Wilkins.
Fourgeaud, J., Mirand, A., Demortier, J., Kamus, L., Collet, L., Olivier, S., Henquell, C., & Vauloup-Fellous, C. (2022). Enterovirus meningitis in Mayotte French Comoros Island, March–June 2019. Journal of Clinical Virology, 150–151, 105154.
pubmed: 35398601
doi: 10.1016/j.jcv.2022.105154
Fratty, I. S., Kriger, O., Weiss, L., Vasserman, R., Erster, O., Mendelson, E., Sofer, D., & Weil, M. (2023). Increased detection of Echovirus 6-associated meningitis in patients hospitalized during the COVID-19 pandemic, Israel 2021–2022. Journal of Clinical Virology, 162, 105425.
pubmed: 37023500
pmcid: 10038676
doi: 10.1016/j.jcv.2023.105425
Garcia-Boronat, M., Diez-Rivero, C. M., Reinherz, E. L., & Reche, P. A. (2008). PVS: A web server for protein sequence variability analysis tuned to facilitate conserved epitope discovery. Nucleic Acids Research, 36, W35–W41.
pubmed: 18442995
pmcid: 2447719
doi: 10.1093/nar/gkn211
Grädel, C., Ireddy, N. R., Koch, M. C., Baumann, C., Terrazos Miani, M. A., Barbani, M. T., Steinlin-Schopfer, J., Suter-Riniker, F., Leib, S. L., & Ramette, A. (2022). Genome sequences of rare human enterovirus genotypes recovered from clinical respiratory samples in Bern. Switzerland. Microbiology Resource Announcements, 11, e0027622.
pubmed: 35993703
doi: 10.1128/mra.00276-22
Grenfell, B. T., Pybus, O. G., Gog, J. R., Wood, J. L., Daly, J. M., Mumford, J. A., & Holmes, E. C. (2004). Unifying the epidemiological and evolutionary dynamics of pathogens. Science, 303, 327–332.
pubmed: 14726583
doi: 10.1126/science.1090727
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Handsher, R., Shulman, L. M., Abramovitz, B., Silberstein, I., Neuman, M., Tepperberg-Oikawa, M., Fisher, T., & Mendelson, E. (1999). A new variant of echovirus 4 associated with a large outbreak of aseptic meningitis. Journal of Clinical Virology, 13, 29–36.
pubmed: 10405889
doi: 10.1016/S1386-6532(99)00014-1
Hirade, T., Abe, Y., Ito, S., Suzuki, T., Katano, H., Takahashi, N., Koike, D., Nariai, A., & Kato, F. (2023). Congenital Echovirus 11 infection in a neonate. The Pediatric Infectious Disease Journal. https://doi.org/10.1097/inf.0000000000004052
doi: 10.1097/inf.0000000000004052
pubmed: 37523578
Home of Picornaviruses. (2023). Enterovirus B. The Pirbright Institute. Retrieved from https://www.picornaviridae.com/ensavirinae/enterovirus/ev-b/ev-b.htm .
Huang, Q. S., Carr, J. M., Nix, W. A., Oberste, M. S., Kilpatrick, D. R., Pallansch, M. A., Croxson, M. C., Lindeman, J. A., Baker, M. G., & Grimwood, K. (2003). An echovirus type 33 winter outbreak in New Zealand. Clinical Infectious Diseases, 37, 650–657.
pubmed: 12942395
doi: 10.1086/376915
ICTV, International Committee on Taxonomy of Viruses. (2023). Taxon Details. Enterovirus B. Retrieved from https://ictv.global/taxonomy/taxondetails?taxnode_id=202101984 (20 Feb 2023).
Jiang, C., Xu, Z., Li, J., Zhang, J., Xue, X., Jiang, J., Jiang, G., Wang, X., Peng, Y., Chen, T., et al. (2022). Case report: Clinical and virological characteristics of aseptic meningitis caused by a recombinant echovirus 18 in an immunocompetent adult. Frontiers in Medicine, 9, 1094347.
pubmed: 36714132
doi: 10.3389/fmed.2022.1094347
Kabat, E. A., Wu, T. T., & Bilofsky, H. (1977). Unusual distributions of amino acids in complementarity determining (hypervariable) segments of heavy and light chains of immunoglobulins and their possible roles in specificity of antibody-combining sites. Journal of Biological Chemistry, 252, 6609–6616.
pubmed: 408353
doi: 10.1016/S0021-9258(17)39891-5
Khetsuriani, N., Lamonte-Fowlkes, A., Oberst, S., Pallansch, M. A., Centers for Disease Control and Prevention. (2006). Enterovirus surveillance—United States, 1970–2005. Morbidity and Mortality Weekly Report. Surveillance Summaries, 55, 1–20.
pubmed: 16971890
Kyriakopoulou, Z., Bletsa, M., Tsakogiannis, D., Dimitriou, T. G., Amoutzias, G. D., Gartzonika, C., Levidiotou-Stefanou, S., & Markoulatos, P. (2015a). Molecular epidemiology and evolutionary dynamics of Echovirus 3 serotype. Infection, Genetics and Evolution, 32, 305–312.
pubmed: 25791929
doi: 10.1016/j.meegid.2015.03.008
Kyriakopoulou, Z., Pliaka, V., Amoutzias, G. D., & Markoulatos, P. (2015b). Recombination among human non-polio enteroviruses: Implications for epidemiology and evolution. Virus Genes, 50, 177–188.
pubmed: 25537948
doi: 10.1007/s11262-014-1152-y
Lavania, M., Viswanathan, R., Bhardwaj, S. D., Oswal, J. S., Chavan, N., Shinde, M., & Katendra, S. (2022). Detection of Echovirus-18 in children suspected With SARS-CoV-2 infection with multisystem inflammatory syndrome: A case report from India. Frontiers in Public Health, 10, 897662.
pubmed: 35937258
pmcid: 9355657
doi: 10.3389/fpubh.2022.897662
Leigh, J. W., & Bryant, D. (2015). POPART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116.
doi: 10.1111/2041-210X.12410
Lema, C., Torres, C., Van der Sanden, S., Cisterna, D., Freire, M. C., & Gómez, R. M. (2019). Global phylodynamics of Echovirus 30 revealed differential behavior among viral lineages. Virology, 531, 79–92.
pubmed: 30856485
doi: 10.1016/j.virol.2019.02.012
Li, J., Yan, D., Chen, L., Zhang, Y., Song, Y., Zhu, S., Ji, T., Zhou, W., Gan, F., Wang, X., Hong, M., Guan, L., Shi, Y., Wu, G., & Xu, W. (2019). Multiple genotypes of Echovirus 11 circulated in mainland China between 1994 and 2017. Scientific Reports, 9, 10583.
pubmed: 31332200
pmcid: 6646367
doi: 10.1038/s41598-019-46870-w
Liu, H., Zhang, J., Zhao, Y., Zhang, H., Lin, K., Sun, H., Huang, X., Yang, Z., & Ma, S. (2018). Molecular characterization of echovirus 12 strains isolated from healthy children in China. Scientific Reports, 8, 11716.
pubmed: 30082917
pmcid: 6078983
doi: 10.1038/s41598-018-30250-x
Lizasoain, A., Mir, D., Victoria, M., Barrios, M. E., Blanco-Fernández, M. D., Rodríguez-Osorio, N., Nates, S., Cisterna, D., Mbayed, V. A., & Colina, R. (2021). Human Enterovirus diversity by next-generation sequencing analysis in urban sewage samples from Buenos Aires Metropolitan Area, Argentina: A retrospective study. Food and Environmental Virology, 13, 259–269.
pubmed: 33675515
doi: 10.1007/s12560-021-09468-y
Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E., & Ilonen, J. (2005). Recombination in circulating Human enterovirus B: Independent evolution of structural and non-structural genome regions. The Journal of General Virology, 86, 3281–3290.
pubmed: 16298973
doi: 10.1099/vir.0.81264-0
Martin, D. P., Murrell, B., Golden, M., Khoosal, A., & Muhire, B. (2015). RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evolution, 1, vev003.
pubmed: 27774277
pmcid: 5014473
doi: 10.1093/ve/vev003
Miyata, I., Hanaoka, N., Okabe, N., Fujimoto, T., Sakamoto, S., Kasahara, M., & Saitoh, A. (2014). Echovirus 3 as another enterovirus causing life-threatening neonatal fulminant hepatitis. Journal of Clinical Virology, 59, 132–134.
pubmed: 24374056
doi: 10.1016/j.jcv.2013.11.015
Morsli, M., Vincent, J. J., Milliere, L., Colson, P., & Drancourt, M. (2021). Direct next-generation sequencing diagnosis of echovirus 9 meningitis, France. European Journal of Clinical Microbiology & Infectious Diseases, 40, 2037–2039.
doi: 10.1007/s10096-021-04205-6
Oberste, M. S., Maher, K., & Pallansch, M. A. (2004). Evidence for frequent recombination within species Human Enterovirus B based on complete genomic sequences of all thirty-seven serotypes. Journal of Virology, 78, 855–867.
pubmed: 14694117
pmcid: 368751
doi: 10.1128/JVI.78.2.855-867.2004
Oberste, M. S., Nix, W. A., Kilpatrick, D. R., Flemister, M. R., & Pallansch, M. A. (2003). Molecular epidemiology and type-specific detection of echovirus 11 isolates from the Americas, Europe, Africa, Australia, southern Asia and the Middle East. Virus Research, 91, 241–248.
pubmed: 12573503
doi: 10.1016/S0168-1702(02)00291-5
Ogbole, O. O., Akinleye, T. E., Segun, P. A., Faleye, T. C., & Adeniji, A. J. (2018). In vitro antiviral activity of twenty-seven medicinal plant extracts from Southwest Nigeria against three serotypes of echoviruses. Virology Journal, 15, 110.
pubmed: 30021589
pmcid: 6052623
doi: 10.1186/s12985-018-1022-7
Paul, A. V., & Wimmer, E. (2015). Initiation of protein-primed picornavirus RNA synthesis. Virus Research, 206, 12–26.
pubmed: 25592245
doi: 10.1016/j.virusres.2014.12.028
Pedrosa, C., Lage, M. J., & Virella, D. (2013). Congenital echovirus 21 infection causing fulminant hepatitis in a neonate. BMJ Case Reports. https://doi.org/10.1136/bcr-2012-008394
doi: 10.1136/bcr-2012-008394
pubmed: 23729699
pmcid: 3670030
Racaniello, V. R. (2007). Picornaviridae: The viruses and their replication. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, & S. E. Strauss (Eds.), Fields virology (5th ed., pp. 795–838). Lippincott Williams & Wilkins.
Ramos-Alvarez, M., & Sabin, A. B. (1954). Characteristics of poliomyelitis and other enteric viruses recovered in tissue culture from healthy American children. Proceedings of the Society for Experimental Biology and Medicine, 87, 655–661.
pubmed: 13237336
doi: 10.3181/00379727-87-21474
Rao, C. D. (2015). Non-polio enteroviruses, the neglected and emerging human pathogens: Are we waiting for the sizzling enterovirus volcano to erupt. Proceedings of the Indian National Science Academy, 81, 447–462.
Roberts, J. A., Hobday, L. K., Ibrahim, A., & Thorley, B. R. (2020). Australian National Enterovirus Reference laboratory annual report 2018. Communicable Diseases Intelligence. https://doi.org/10.33321/cdi.2020.44.26
doi: 10.33321/cdi.2020.44.26
pubmed: 33349203
Rueca, M., Lanini, S., Giombini, E., Messina, F., Castilletti, C., Ippolito, G., Capobianchi, M. R., & Valli, M. B. (2022). Detection of recombinant breakpoint in the genome of human enterovirus E11 strain associated with a fatal nosocomial outbreak. Virol Journal, 19, 97.
doi: 10.1186/s12985-022-01821-2
Shaukat, S., Angez, M., Mahmood, T., Alam, M. M., Sharif, S., Khurshid, A., Rana, M. S., & Zaidi, S. S. (2017). Molecular characterization of echovirus 13 uncovering high genetic diversity and identification of new genotypes in Pakistan. Infection, Genetics and Evolution, 48, 102–108.
pubmed: 28011278
doi: 10.1016/j.meegid.2016.12.017
Sousa, I. P., Jr., Burlandy, F. M., Lima, S. T. S., Maximo, A. C. B., Figueiredo, M. A. A., Maia, Z., & da Silva, E. E. (2019). Echovirus 30 detection in an outbreak of acute myalgia and rhabdomyolysis, Brazil 2016–2017. Clinical Microbiology and Infection, 25, 252.e2-252.e8.
doi: 10.1016/j.cmi.2018.08.018
Sun, Y., Miao, Z., Yan, J., Gong, L., Chen, Y., Chen, Y., Mao, H., & Zhang, Y. (2019). Sero-molecular epidemiology of enterovirus-associated encephalitis in Zhejiang Province, China, from 2014 to 2017. International Journal of Infectious Diseases, 79, 58–64.
pubmed: 30423458
doi: 10.1016/j.ijid.2018.11.002
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022–3027.
pubmed: 33892491
pmcid: 8233496
doi: 10.1093/molbev/msab120
Trifinopoulos, J., Nguyen, L. T., von Haeseler, A., & Minh, B. Q. (2016). W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44, W232–W235.
pubmed: 27084950
pmcid: 4987875
doi: 10.1093/nar/gkw256
Wieczorek, M., Krzysztoszek, A., Ciąćka, A., & Figas, A. (2017). Molecular characterization of environmental and clinical echovirus 6 isolates from Poland, 2006–2014. Journal of Medical Virology, 89, 936–940.
pubmed: 27736044
doi: 10.1002/jmv.24709
Xi, H., Tian, Y., Shao, H., Yin, X., Ma, L., Yang, P., & Li, X. (2023). An outbreak of nosocomial infection of neonatal aseptic meningitis caused by echovirus 18. Epidemiology and Infection, 151, e107.
pubmed: 37311733
pmcid: 10369423
doi: 10.1017/S0950268823000973
Xiao, J., Zhang, Y., Hong, M., Han, Z., Zhang, M., Song, Y., Yan, D., Zhu, S., & Xu, W. (2020). Phylogenetic characteristics and molecular epidemiological analysis of novel enterovirus EV-B83 isolated from Tibet, China. Scientific Reports, 10, 6630.
pubmed: 32313119
pmcid: 7171079
doi: 10.1038/s41598-020-63691-4
Yao, X., Bian, L. L., Mao, Q. Y., Zhu, F. C., Ye, Q., & Liang, Z. L. (2015). Echovirus 7 associated with hand, foot, and mouth disease in mainland China has undergone a recombination event. Archives of Virology, 160, 1291–1295.
pubmed: 25680567
pmcid: 4412592
doi: 10.1007/s00705-015-2350-1
Zhang, D., Lu, J., & Lu, J. (2010). Enterovirus 71 vaccine: Close but still far. International Journal of Infectious Diseases, 14, e739–e743.
pubmed: 20400350
pmcid: 7110504
doi: 10.1016/j.ijid.2009.12.002
Zhang, M., Guo, W., Xu, D., Feng, C., Bao, G., Sun, H., Yang, Z., & Ma, S. (2022). Molecular characterization of echovirus 9 strains isolated from hand-foot-and-mouth disease in Kunming, Yunnan Province. China. Scientific Reports, 12, 2293.
pubmed: 35145190
doi: 10.1038/s41598-022-06309-1
Zhu, Y., Zhou, X., Liu, J., Xia, L., Pan, Y., Chen, J., Luo, N., Yin, J., & Ma, S. (2016). Molecular identification of human enteroviruses associated with aseptic meningitis in Yunnan province, Southwest China. Springerplus, 5, 1515.
pubmed: 27652088
pmcid: 5016492
doi: 10.1186/s40064-016-3194-1