Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus

Canine distemper virus (CDV) is a worldwide distributed virus which belongs to the genus Morbillivirus within the Paramyxoviridae family. CDV spreads through the lymphatic, epithelial, and nervous systems of domestic dogs and wildlife, in at least six orders and over 20 families of mammals. Due to t...

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Autores:
Ruiz Sáenz, Julián
Duque Valencia, July
Sarute, Nicolás
Olarte Castillo, Ximena
Tipo de recurso:
Article of journal
Fecha de publicación:
2019
Institución:
Universidad Cooperativa de Colombia
Repositorio:
Repositorio UCC
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oai:repository.ucc.edu.co:20.500.12494/15174
Acceso en línea:
https://hdl.handle.net/20.500.12494/15174
Palabra clave:
Canine distemper virus
genome evolution
genotype
hemagglutinin gene
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openAccess
License
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dc.title.spa.fl_str_mv Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
title Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
spellingShingle Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
Canine distemper virus
genome evolution
genotype
hemagglutinin gene
title_short Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
title_full Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
title_fullStr Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
title_full_unstemmed Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
title_sort Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus
dc.creator.fl_str_mv Ruiz Sáenz, Julián
Duque Valencia, July
Sarute, Nicolás
Olarte Castillo, Ximena
dc.contributor.author.none.fl_str_mv Ruiz Sáenz, Julián
Duque Valencia, July
Sarute, Nicolás
Olarte Castillo, Ximena
dc.subject.spa.fl_str_mv Canine distemper virus
genome evolution
genotype
hemagglutinin gene
topic Canine distemper virus
genome evolution
genotype
hemagglutinin gene
description Canine distemper virus (CDV) is a worldwide distributed virus which belongs to the genus Morbillivirus within the Paramyxoviridae family. CDV spreads through the lymphatic, epithelial, and nervous systems of domestic dogs and wildlife, in at least six orders and over 20 families of mammals. Due to the high morbidity and mortality rates and broad host range, understanding the epidemiology of CDV is not only important for its control in domestic animals, but also for the development of reliable wildlife conservation strategies. The present review aims to give an outlook of the multiple evolutionary landscapes and factors involved in the transmission of CDV by including epidemiological data from multiple species in urban, wild and peri-urban settings, not only in domestic animal populations but at the wildlife interface. It is clear that different epidemiological scenarios can lead to the presence of CDV in wildlife even in the absence of infection in domestic populations, highlighting the role of CDV in different domestic or wild species without clinical signs of disease mainly acting as reservoirs (peridomestic and mesocarnivores) that are often found in peridomestic habits triggering CDV epidemics. Another scenario is driven by mutations, which generate genetic variation on which random drift and natural selection can act, shaping the genetic structure of CDV populations leading to some fitness compensations between hosts and driving the evolution of specialist and generalist traits in CDV populations. In this scenario, the highly variable protein hemagglutinin (H) determines the cellular and host tropism by binding to signaling lymphocytic activation molecule (SLAM) and nectin-4 receptors of the host; however, the multiple evolutionary events that may have facilitated CDV adaptation to different hosts must be evaluated by complete genome sequencing. This review is focused on the study of CDV interspecies transmission by examining molecular and epidemiological reports based on sequences of the hemagglutinin gene and the growing body of studies of the complete genome; emphasizing the importance of long-term multidisciplinary research that tracks CDV in the presence or absence of clinical signs in wild species, and helping to implement strategies to mitigate the infection. Integrated research incorporating the experience of wildlife managers, behavioral and conservation biologists, veterinarians, virologists, and immunologists (among other scientific areas) and the inclusion of several wild and domestic species is essential for understanding the intricate epidemiological dynamics of CDV in its multiple host infections.
publishDate 2019
dc.date.accessioned.none.fl_str_mv 2019-11-20T21:07:12Z
dc.date.available.none.fl_str_mv 2019-11-20T21:07:12Z
dc.date.issued.none.fl_str_mv 2019-06-26
dc.type.none.fl_str_mv Artículo
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dc.identifier.bibliographicCitation.spa.fl_str_mv Duque-Valencia J, Sarute N, Olarte-Castillo X. A., Ruíz-Sáenz J. (2019) Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus. Viruses. 2019 Jun 26;11(7). pii: E582. doi: 10.3390/v11070582.
identifier_str_mv 1999-4915
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Duque-Valencia J, Sarute N, Olarte-Castillo X. A., Ruíz-Sáenz J. (2019) Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus. Viruses. 2019 Jun 26;11(7). pii: E582. doi: 10.3390/v11070582.
url https://hdl.handle.net/20.500.12494/15174
dc.relation.isversionof.spa.fl_str_mv https://www.mdpi.com/1999-4915/11/7/582
dc.relation.ispartofjournal.spa.fl_str_mv Viruses.
dc.relation.references.spa.fl_str_mv MacLachlan N., Dubovi E., Fenner F. Fenner’s Veterinary Virology. 4th ed. Academic Press; Boston, MA, USA: 2011. Paramyxoviridae; pp. 299–325
King A.M.Q., Lefkowitz E.J., Mushegian A.R., Adams M.J., Dutilh B.E., Gorbalenya A.E., Harrach B., Harrison R.L., Junglen S., Knowles N.J., et al. Changes to taxonomy and the international code of virus classification and nomenclature ratified by the international committee on taxonomy of viruses (2018) Arch. Virol. 2018;163:2601–2631. doi: 10.1007/s00705-018-3847-1.
Martinez-Gutierrez M., Ruiz-Saenz J. Diversity of susceptible hosts in canine distemper virus infection: A systematic review and data synthesis. BMC Vet. Res. 2016;12:78. doi: 10.1186/s12917-016-0702-z
Loots A.K., Mitchell E., Dalton D.L., Kotze A., Venter E.H. Advances in canine distemper virus pathogenesis research: A wildlife perspective. J. Gen. Virol. 2017;98:311–321. doi: 10.1099/jgv.0.000666.
Anderson D.E., Von Messling V. Region between the canine distemper virus M and F genes modulates virulence by controlling fusion protein expression. J. Virol. 2008;82:10510–10518. doi: 10.1128/JVI.01419-08.
Wolfe N.D., Dunavan C.P., Diamond J. Origins of major human infectious diseases. Nature. 2007;447:279–283. doi: 10.1038/nature05775.
Schuhmann K.M., Pfaller C.K., Conzelmann K.K. The measles virus V protein binds to p65 (Rela) to suppress NF-kappaB activity. J. Virol. 2011;85:3162–3171. doi: 10.1128/JVI.02342-10
hinnakannan S.K., Nanda S.K., Baron M.D. Morbillivirus v proteins exhibit multiple mechanisms to block type 1 and type 2 interferon signalling pathways. PLoS ONE. 2013;8:e57063. doi: 10.1371/journal.pone.0057063.
Rothlisberger A., Wiener D., Schweizer M., Peterhans E., Zurbriggen A., Plattet P. Two domains of the v protein of virulent canine distemper virus selectively inhibit stat1 and stat2 nuclear import. J. Virol. 2010;84:6328–6343. doi: 10.1128/JVI.01878-09.
Svitek N., Gerhauser I., Goncalves C., Grabski E., Döring M., Kalinke U., Anderson D.E., Cattaneo R., Von Messling V. Morbillivirus control of the interferon response: Relevance of stat2 and mda5 but not stat1 for canine distemper virus virulence in ferrets. J. Virol. 2013;88:2941–2950. doi: 10.1128/JVI.03076-13.
Pomeroy L.W., Bjornstad O.N., Holmes E.C. The evolutionary and epidemiological dynamics of the paramyxoviridae. J. Mol. Evol. 2008;66:98–106. doi: 10.1007/s00239-007-9040-x
Sarkar J., Balamurugan V., Sen A., Saravanan P., Sahay B., Rajak K.K., Rasool T.J., Bhanuprakash V., Singh R.K. Sequence analysis of morbillivirus CD150 receptor-signaling lymphocyte activation molecule (SLAM) of different animal species. Virus Genes. 2009;39:335–341. doi: 10.1007/s11262-009-0391-9.
Tatsuo H., Yanagi Y. The morbillivirus receptor SLAM (CD150) Microbiol. Immunol. 2002;46:135–142. doi: 10.1111/j.1348-0421.2002.tb02678.x. [
Noyce R.S., Bondre D.G., Ha M.N., Lin L.-T., Sisson G., Tsao M.-S., Richardson C.D. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 2011;7:e1002240. doi: 10.1371/journal.ppat.1002240
Schultz R.D., Thiel B., Mukhtar E., Sharp P., Larson L.J. Age and long-term protective immunity in dogs and cats. J. Comp. Pathol. 2010;142:S102–S108. doi: 10.1016/j.jcpa.2009.10.009.
Bolt G., Jensen T.D., Gottschalck E., Arctander P., Appel M.J., Buckland R., Blixenkrone-Moller M. Genetic diversity of the attachment (H) protein gene of current field isolates of canine distemper virus. J. Gen. Virol. 1997;78:367–372. doi: 10.1099/0022-1317-78-2-367.
Russell C.J., Jardetzky T.S., Lamb R.A. Membrane fusion machines of paramyxoviruses: Capture of intermediates of fusion. EMBO J. 2001;20:4024–4034. doi: 10.1093/emboj/20.15.4024.
Bringolf F., Herren M., Wyss M., Vidondo B., Langedijk J.P., Zurbriggen A., Plattet P. Dimerization efficiency of canine distemper virus matrix protein regulates membrane-budding activity. J. Virol. 2017;91 doi: 10.1128/JVI.00521-17
Sarute N., Calderon M.G., Perez R., La Torre J., Hernandez M., Francia L., Panzera Y. The fusion protein signal-peptide-coding region of canine distemper virus: A useful tool for phylogenetic reconstruction and lineage identification. PLoS ONE. 2013;8:e63595. doi: 10.1371/journal.pone.0063595.
Elia G., Camero M., Losurdo M., Lucente M.S., Larocca V., Martella V., Decaro N., Buonavoglia C. Virological and serological findings in dogs with naturally occurring distemper. J. Virol. Methods. 2015;213:127–130. doi: 10.1016/j.jviromet.2014.12.004.
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spelling Ruiz Sáenz, JuliánDuque Valencia, JulySarute, NicolásOlarte Castillo, Ximena11(7).2019-11-20T21:07:12Z2019-11-20T21:07:12Z2019-06-261999-4915doi: 10.3390/v11070582.https://hdl.handle.net/20.500.12494/15174Duque-Valencia J, Sarute N, Olarte-Castillo X. A., Ruíz-Sáenz J. (2019) Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus. Viruses. 2019 Jun 26;11(7). pii: E582. doi: 10.3390/v11070582.Canine distemper virus (CDV) is a worldwide distributed virus which belongs to the genus Morbillivirus within the Paramyxoviridae family. CDV spreads through the lymphatic, epithelial, and nervous systems of domestic dogs and wildlife, in at least six orders and over 20 families of mammals. Due to the high morbidity and mortality rates and broad host range, understanding the epidemiology of CDV is not only important for its control in domestic animals, but also for the development of reliable wildlife conservation strategies. The present review aims to give an outlook of the multiple evolutionary landscapes and factors involved in the transmission of CDV by including epidemiological data from multiple species in urban, wild and peri-urban settings, not only in domestic animal populations but at the wildlife interface. It is clear that different epidemiological scenarios can lead to the presence of CDV in wildlife even in the absence of infection in domestic populations, highlighting the role of CDV in different domestic or wild species without clinical signs of disease mainly acting as reservoirs (peridomestic and mesocarnivores) that are often found in peridomestic habits triggering CDV epidemics. Another scenario is driven by mutations, which generate genetic variation on which random drift and natural selection can act, shaping the genetic structure of CDV populations leading to some fitness compensations between hosts and driving the evolution of specialist and generalist traits in CDV populations. In this scenario, the highly variable protein hemagglutinin (H) determines the cellular and host tropism by binding to signaling lymphocytic activation molecule (SLAM) and nectin-4 receptors of the host; however, the multiple evolutionary events that may have facilitated CDV adaptation to different hosts must be evaluated by complete genome sequencing. This review is focused on the study of CDV interspecies transmission by examining molecular and epidemiological reports based on sequences of the hemagglutinin gene and the growing body of studies of the complete genome; emphasizing the importance of long-term multidisciplinary research that tracks CDV in the presence or absence of clinical signs in wild species, and helping to implement strategies to mitigate the infection. Integrated research incorporating the experience of wildlife managers, behavioral and conservation biologists, veterinarians, virologists, and immunologists (among other scientific areas) and the inclusion of several wild and domestic species is essential for understanding the intricate epidemiological dynamics of CDV in its multiple host infections.http://scienti.colciencias.gov.co:8081/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0000153095https://orcid.org/0000-0002-1447-1458julian.ruizs@campusucc.edu.cohttps://scholar.google.com/citations?user=o3Y7mZwAAAAJ&hl=esUniversidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Medicina Veterinaría y Zootecnia, BucaramangaMDPIMedicina veterinaria y zootecniaBucaramangahttps://www.mdpi.com/1999-4915/11/7/582Viruses.MacLachlan N., Dubovi E., Fenner F. Fenner’s Veterinary Virology. 4th ed. Academic Press; Boston, MA, USA: 2011. Paramyxoviridae; pp. 299–325King A.M.Q., Lefkowitz E.J., Mushegian A.R., Adams M.J., Dutilh B.E., Gorbalenya A.E., Harrach B., Harrison R.L., Junglen S., Knowles N.J., et al. Changes to taxonomy and the international code of virus classification and nomenclature ratified by the international committee on taxonomy of viruses (2018) Arch. Virol. 2018;163:2601–2631. doi: 10.1007/s00705-018-3847-1.Martinez-Gutierrez M., Ruiz-Saenz J. Diversity of susceptible hosts in canine distemper virus infection: A systematic review and data synthesis. BMC Vet. Res. 2016;12:78. doi: 10.1186/s12917-016-0702-zLoots A.K., Mitchell E., Dalton D.L., Kotze A., Venter E.H. Advances in canine distemper virus pathogenesis research: A wildlife perspective. J. Gen. Virol. 2017;98:311–321. doi: 10.1099/jgv.0.000666.Anderson D.E., Von Messling V. Region between the canine distemper virus M and F genes modulates virulence by controlling fusion protein expression. J. Virol. 2008;82:10510–10518. doi: 10.1128/JVI.01419-08.Wolfe N.D., Dunavan C.P., Diamond J. Origins of major human infectious diseases. Nature. 2007;447:279–283. doi: 10.1038/nature05775.Schuhmann K.M., Pfaller C.K., Conzelmann K.K. The measles virus V protein binds to p65 (Rela) to suppress NF-kappaB activity. J. Virol. 2011;85:3162–3171. doi: 10.1128/JVI.02342-10hinnakannan S.K., Nanda S.K., Baron M.D. Morbillivirus v proteins exhibit multiple mechanisms to block type 1 and type 2 interferon signalling pathways. PLoS ONE. 2013;8:e57063. doi: 10.1371/journal.pone.0057063.Rothlisberger A., Wiener D., Schweizer M., Peterhans E., Zurbriggen A., Plattet P. Two domains of the v protein of virulent canine distemper virus selectively inhibit stat1 and stat2 nuclear import. J. Virol. 2010;84:6328–6343. doi: 10.1128/JVI.01878-09.Svitek N., Gerhauser I., Goncalves C., Grabski E., Döring M., Kalinke U., Anderson D.E., Cattaneo R., Von Messling V. Morbillivirus control of the interferon response: Relevance of stat2 and mda5 but not stat1 for canine distemper virus virulence in ferrets. J. Virol. 2013;88:2941–2950. doi: 10.1128/JVI.03076-13.Pomeroy L.W., Bjornstad O.N., Holmes E.C. The evolutionary and epidemiological dynamics of the paramyxoviridae. J. Mol. Evol. 2008;66:98–106. doi: 10.1007/s00239-007-9040-xSarkar J., Balamurugan V., Sen A., Saravanan P., Sahay B., Rajak K.K., Rasool T.J., Bhanuprakash V., Singh R.K. Sequence analysis of morbillivirus CD150 receptor-signaling lymphocyte activation molecule (SLAM) of different animal species. Virus Genes. 2009;39:335–341. doi: 10.1007/s11262-009-0391-9.Tatsuo H., Yanagi Y. The morbillivirus receptor SLAM (CD150) Microbiol. Immunol. 2002;46:135–142. doi: 10.1111/j.1348-0421.2002.tb02678.x. [Noyce R.S., Bondre D.G., Ha M.N., Lin L.-T., Sisson G., Tsao M.-S., Richardson C.D. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 2011;7:e1002240. doi: 10.1371/journal.ppat.1002240Schultz R.D., Thiel B., Mukhtar E., Sharp P., Larson L.J. Age and long-term protective immunity in dogs and cats. J. Comp. Pathol. 2010;142:S102–S108. doi: 10.1016/j.jcpa.2009.10.009.Bolt G., Jensen T.D., Gottschalck E., Arctander P., Appel M.J., Buckland R., Blixenkrone-Moller M. Genetic diversity of the attachment (H) protein gene of current field isolates of canine distemper virus. J. Gen. Virol. 1997;78:367–372. doi: 10.1099/0022-1317-78-2-367.Russell C.J., Jardetzky T.S., Lamb R.A. Membrane fusion machines of paramyxoviruses: Capture of intermediates of fusion. EMBO J. 2001;20:4024–4034. doi: 10.1093/emboj/20.15.4024.Bringolf F., Herren M., Wyss M., Vidondo B., Langedijk J.P., Zurbriggen A., Plattet P. Dimerization efficiency of canine distemper virus matrix protein regulates membrane-budding activity. J. Virol. 2017;91 doi: 10.1128/JVI.00521-17Sarute N., Calderon M.G., Perez R., La Torre J., Hernandez M., Francia L., Panzera Y. The fusion protein signal-peptide-coding region of canine distemper virus: A useful tool for phylogenetic reconstruction and lineage identification. PLoS ONE. 2013;8:e63595. doi: 10.1371/journal.pone.0063595.Elia G., Camero M., Losurdo M., Lucente M.S., Larocca V., Martella V., Decaro N., Buonavoglia C. Virological and serological findings in dogs with naturally occurring distemper. J. Virol. Methods. 2015;213:127–130. doi: 10.1016/j.jviromet.2014.12.004.Canine distemper virusgenome evolutiongenotypehemagglutinin geneEvolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host 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