Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells
Canine morbillivirus (CDV) is a viral agent that infects domestic dogs and a vast array of wildlife species. It belongs to the Paramyxoviridae family, genus Morbillivirus, which is shared with the Measles virus (MeV). Both viruses employ orthologous cellular receptors, SLAM in mononuclear cells and...
- Autores:
-
Rendón Marín, Santiago
Quintero Gil, Carolina
Guerra, Diego
Muskus, Carlos
Ruiz Sáenz, Julián
- Tipo de recurso:
- Article of investigation
- Fecha de publicación:
- 2021
- Institución:
- Universidad Cooperativa de Colombia
- Repositorio:
- Repositorio UCC
- Idioma:
- OAI Identifier:
- oai:repository.ucc.edu.co:20.500.12494/43971
- Acceso en línea:
- https://hdl.handle.net/20.500.12494/43971
- Palabra clave:
- Canine distemper
Cellular receptor
Inter-species transmission
Nectin-4
SLAM molecule
- Rights
- openAccess
- License
- Atribución – No comercial – Compartir igual
| id |
COOPER2_3c607334b2f7b82dae7413249bf645ee |
|---|---|
| oai_identifier_str |
oai:repository.ucc.edu.co:20.500.12494/43971 |
| network_acronym_str |
COOPER2 |
| network_name_str |
Repositorio UCC |
| repository_id_str |
|
| dc.title.spa.fl_str_mv |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells |
| title |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells |
| spellingShingle |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells Canine distemper Cellular receptor Inter-species transmission Nectin-4 SLAM molecule |
| title_short |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells |
| title_full |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells |
| title_fullStr |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells |
| title_full_unstemmed |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells |
| title_sort |
Canine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cells |
| dc.creator.fl_str_mv |
Rendón Marín, Santiago Quintero Gil, Carolina Guerra, Diego Muskus, Carlos Ruiz Sáenz, Julián |
| dc.contributor.author.none.fl_str_mv |
Rendón Marín, Santiago Quintero Gil, Carolina Guerra, Diego Muskus, Carlos Ruiz Sáenz, Julián |
| dc.subject.spa.fl_str_mv |
Canine distemper Cellular receptor Inter-species transmission Nectin-4 SLAM molecule |
| topic |
Canine distemper Cellular receptor Inter-species transmission Nectin-4 SLAM molecule |
| description |
Canine morbillivirus (CDV) is a viral agent that infects domestic dogs and a vast array of wildlife species. It belongs to the Paramyxoviridae family, genus Morbillivirus, which is shared with the Measles virus (MeV). Both viruses employ orthologous cellular receptors, SLAM in mononuclear cells and Nectin-4 in epithelial cells, to enter the cells. Although CDV and MeV hemagglutinin (H) have similar functions in viral pathogenesis and cell tropism, the potential interaction of CDV-H protein with human cellular receptors is still uncertain. Considering that CDV is classified as a multi-host pathogen, the potential risk of CDV transmission to humans has not been fully discarded. In this study, we aimed to evaluate both in silico and in vitro, whether there is a cross-species transmission potential from CDV to humans. To accomplish this, the CDV-H protein belonging to the Colombian lineage was modelled. After model validations, molecular docking and molecular dynamics simulations were carried out between Colombian CDV-H protein and canine and human cellular receptors to determine different aspects of the protein–protein interactions. Moreover, cell lines expressing orthologous cellular receptors, with both reference and wild-type CDV strains, were conducted to determine the CDV cross-species transmission potential from an in vitro model. This in silico and in vitro approach suggests the possibility that CDV interacts with ortholog human SLAM (hSLAM) and human Nectin-4 receptors to infect human cell lines, which could imply a potential cross-species transmission of CDV from dogs to humans. |
| publishDate |
2021 |
| dc.date.issued.none.fl_str_mv |
2021-09 |
| dc.date.accessioned.none.fl_str_mv |
2022-02-15T20:17:58Z |
| dc.date.available.none.fl_str_mv |
2022-02-15T20:17:58Z |
| dc.type.none.fl_str_mv |
Artículos Científicos |
| dc.type.coar.none.fl_str_mv |
http://purl.org/coar/resource_type/c_2df8fbb1 |
| dc.type.coarversion.none.fl_str_mv |
http://purl.org/coar/version/c_970fb48d4fbd8a85 |
| dc.type.driver.none.fl_str_mv |
info:eu-repo/semantics/article |
| dc.type.version.none.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
| format |
http://purl.org/coar/resource_type/c_2df8fbb1 |
| status_str |
publishedVersion |
| dc.identifier.issn.spa.fl_str_mv |
2076-0817 |
| dc.identifier.uri.spa.fl_str_mv |
doi.org/10.3390/pathogens10091199 |
| dc.identifier.uri.none.fl_str_mv |
https://hdl.handle.net/20.500.12494/43971 |
| dc.identifier.bibliographicCitation.spa.fl_str_mv |
Rendon-Marin, S.; Quintero-Gil, C.; Guerra, D.; Muskus, C.; Ruiz-Saenz, J. Canine Morbillivirus from Colombian Lineage Exhibits In Silico and In Vitro Potential to Infect Human Cells. Pathogens 2021, 10, 1199. https://doi.org/10.3390/pathogens10091199 |
| identifier_str_mv |
2076-0817 doi.org/10.3390/pathogens10091199 Rendon-Marin, S.; Quintero-Gil, C.; Guerra, D.; Muskus, C.; Ruiz-Saenz, J. Canine Morbillivirus from Colombian Lineage Exhibits In Silico and In Vitro Potential to Infect Human Cells. Pathogens 2021, 10, 1199. https://doi.org/10.3390/pathogens10091199 |
| url |
https://hdl.handle.net/20.500.12494/43971 |
| dc.relation.isversionof.spa.fl_str_mv |
https://www.mdpi.com/2076-0817/10/9/1199 |
| dc.relation.ispartofjournal.spa.fl_str_mv |
Pathogens |
| dc.relation.references.spa.fl_str_mv |
MacLachlan, N.; Dubovi, E.; Fenner, F. Fenner’s Veterinary Virology, 4th ed.; Elsevier: Amsterdam, The Netherlands, 2011; pp. 299–325. 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. da Fontoura Budaszewski, R.; Streck, A.F.; Nunes Weber, M.; Maboni Siqueira, F.; Muniz Guedes, R.L.; Wageck Canal, C. Influence of vaccine strains on the evolution of canine distemper virus. Infect. Genet. Evol. 2016, 41, 262–269 Lamb, R.A.; Parks, G.D. Paramyxoviridae. In Fields Virology, 6th ed.; Wolters Kluwer Health Adis (ESP): Philadelphia, PA, USA, 2013 von Messling, V.; Zimmer, G.; Herrler, G.; Haas, L.; Cattaneo, R. The hemagglutinin of canine distemper virus determines tropism and cytopathogenicity. J. Virol. 2001, 75, 6418–6427. von Messling, V.; Oezguen, N.; Zheng, Q.; Vongpunsawad, S.; Braun, W.; Cattaneo, R. Nearby clusters of hemagglutinin residues sustain SLAM-dependent canine distemper virus entry in peripheral blood mononuclear cells. J. Virol. 2005, 79, 5857–5862. Pratakpiriya, W.; Seki, F.; Otsuki, N.; Sakai, K.; Fukuhara, H.; Katamoto, H.; Hirai, T.; Maenaka, K.; Techangamsuwan, S.; Lan, N.T.; et al. Nectin4 is an epithelial cell receptor for canine distemper virus and involved in neurovirulence. J. Virol. 2012, 86, 10207–10210 da Fontoura Budaszewski, R.; von Messling, V. Morbillivirus Experimental Animal Models: Measles Virus Pathogenesis Insights from Canine Distemper Virus. Viruses 2016, 8, 274. 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. Tatsuo, H.; Ono, N.; Yanagi, Y. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J. Virol. 2001, 75, 5842–5850 Rendon-Marin, S.; da Fontoura Budaszewski, R.; Canal, C.W.; Ruiz-Saenz, J. Tropism and molecular pathogenesis of canine distemper virus. Virol. J. 2019, 16, 30. Langedijk, J.P.; Janda, J.; Origgi, F.C.; Orvell, C.; Vandevelde, M.; Zurbriggen, A.; Plattet, P. Canine distemper virus infects canine keratinocytes and immune cells by using overlapping and distinct regions located on one side of the attachment protein. J. Virol. 2011, 85, 11242–11254. Duque-Valencia, J.; Sarute, N.; Olarte-Castillo, X.A.; Ruiz-Saenz, J. Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus. Viruses 2019, 11, 582. Mochizuki, M.; Hashimoto, M.; Hagiwara, S.; Yoshida, Y.; Ishiguro, S. Genotypes of canine distemper virus determined by analysis of the hemagglutinin genes of recent isolates from dogs in Japan. J. Clin. Microbiol. 1999, 37, 2936–2942 Anis, E.; Newell, T.K.; Dyer, N.; Wilkes, R.P. Phylogenetic analysis of the wild-type strains of canine distemper virus circulating in the United States. Virol. J. 2018, 15, 118 Blixenkrone-Moller, M.; Svansson, V.; Appel, M.; Krogsrud, J.; Have, P.; Orvell, C. Antigenic relationships between field isolates of morbilliviruses from different carnivores. Arch. Virol. 1992, 123, 279–294. Espinal, M.A.; Diaz, F.J.; Ruiz-Saenz, J. Phylogenetic evidence of a new canine distemper virus lineage among domestic dogs in Colombia, South America. Vet. Microbiol. 2014, 172, 168–176. Haas, L.; Martens, W.; Greiser-Wilke, I.; Mamaev, L.; Butina, T.; Maack, D.; Barrett, T. Analysis of the haemagglutinin gene of current wild-type canine distemper virus isolates from Germany. Virus Res. 1997, 48, 165–171 Harder, T.C.; Kenter, M.; Vos, H.; Siebelink, K.; Huisman, W.; van Amerongen, G.; Orvell, C.; Barrett, T.; Appel, M.J.; Osterhaus, A.D. Canine distemper virus from diseased large felids: Biological properties and phylogenetic relationships. J. Gen. Virol. 1996, 77, 397–405 Iwatsuki, K.; Tokiyoshi, S.; Hirayama, N.; Nakamura, K.; Ohashi, K.; Wakasa, C.; Mikami, T.; Kai, C. Antigenic differences in the H proteins of canine distemper viruses. Vet. Microbiol. 2000, 71, 281–286. Panzera, Y.; Calderon, M.G.; Sarute, N.; Guasco, S.; Cardeillac, A.; Bonilla, B.; Hernandez, M.; Francia, L.; Bedo, G.; La Torre, J.; et al. Evidence of two co-circulating genetic lineages of canine distemper virus in South America. Virus Res. 2012, 163, 401–404. Riley, M.C.; Wilkes, R.P. Sequencing of emerging canine distemper virus strain reveals new distinct genetic lineage in the United States associated with disease in wildlife and domestic canine populations. Virol. J. 2015, 12, 219. Nikolin, V.M.; Olarte-Castillo, X.A.; Osterrieder, N.; Hofer, H.; Dubovi, E.; Mazzoni, C.J.; Brunner, E.; Goller, K.V.; Fyumagwa, R.D.; Moehlman, P.D.; et al. Canine distemper virus in the Serengeti ecosystem: Molecular adaptation to different carnivore species. Mol. Ecol. 2017, 26, 2111–2130. Zhao, J.J.; Yan, X.J.; Chai, X.L.; Martella, V.; Luo, G.L.; Zhang, H.L.; Gao, H.; Liu, Y.X.; Bai, X.; Zhang, L.; et al. Phylogenetic analysis of the haemagglutinin gene of canine distemper virus strains detected from breeding foxes, raccoon dogs and minks in China. Vet. Microbiol. 2010, 140, 34–42. Radtanakatikanon, A.; Keawcharoen, J.; Charoenvisal, N.T.; Poovorawan, Y.; Prompetchara, E.; Yamaguchi, R.; Techangamsuwan, S. Genotypic lineages and restriction fragment length polymorphism of canine distemper virus isolates in Thailand. Vet. Microbiol. 2013, 166, 76–83. Duque-Valencia, J.; Forero-Munoz, N.R.; Diaz, F.J.; Martins, E.; Barato, P.; Ruiz-Saenz, J. Phylogenetic evidence of the intercontinental circulation of a Canine distemper virus lineage in the Americas. Sci. Rep. 2019, 9, 15747 Duque-Valencia, J.; Diaz, F.J.; Ruiz-Saenz, J. Phylogenomic Analysis of Two Co-Circulating Canine Distemper Virus Lineages in Colombia. Pathogens 2019, 9, 26 Ke, G.M.; Ho, C.H.; Chiang, M.J.; Sanno-Duanda, B.; Chung, C.S.; Lin, M.Y.; Shi, Y.Y.; Yang, M.H.; Tyan, Y.C.; Liao, P.C.; et al. Phylodynamic analysis of the canine distemper virus hemagglutinin gene. BMC Vet. Res. 2015, 11, 164 Hashiguchi, T.; Ose, T.; Kubota, M.; Maita, N.; Kamishikiryo, J.; Maenaka, K.; Yanagi, Y. Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat. Struct. Mol. Biol. 2011, 18, 135–141. Zhang, X.; Lu, G.; Qi, J.; Li, Y.; He, Y.; Xu, X.; Shi, J.; Zhang, C.W.; Yan, J.; Gao, G.F. Structure of measles virus hemagglutinin bound to its epithelial receptor nectin-4. Nat. Struct. Mol. Biol. 2013, 20, 67–72. Yoshikawa, Y.; Ochikubo, F.; Matsubara, Y.; Tsuruoka, H.; Ishii, M.; Shirota, K.; Nomura, Y.; Sugiyama, M.; Yamanouchi, K. Natural infection with canine distemper virus in a Japanese monkey (Macaca fuscata). Vet. Microbiol. 1989, 20, 193–205. Otsuki, N.; Nakatsu, Y.; Kubota, T.; Sekizuka, T.; Seki, F.; Sakai, K.; Kuroda, M.; Yamaguchi, R.; Takeda, M. The V protein of canine distemper virus is required for virus replication in human epithelial cells. PLoS ONE 2013, 8, e82343 Fukuhara, H.; Ito, Y.; Sako, M.; Kajikawa, M.; Yoshida, K.; Seki, F.; Mwaba, M.H.; Hashiguchi, T.; Higashibata, M.A.; Ose, T.; et al. Specificity of Morbillivirus Hemagglutinins to Recognize SLAM of Different Species. Viruses 2019, 11, 761 Bieringer, M.; Han, J.W.; Kendl, S.; Khosravi, M.; Plattet, P.; Schneider-Schaulies, J. Experimental adaptation of wild-type canine distemper virus (CDV) to the human entry receptor CD150. PLoS ONE 2013, 8, e57488 Krieger, E.; Nabuurs, S.B.; Vriend, G. Homology modeling. Methods Biochem. Anal. 2003, 44, 509–523 Quintero-Gil, C.; Rendon-Marin, S.; Martinez-Gutierrez, M.; Ruiz-Saenz, J. Origin of Canine Distemper Virus: Consolidating Evidence to Understand Potential Zoonoses. Front. Microbiol. 2019, 10, 1982. Cosby, S.L.; Weir, L. Measles vaccination: Threat from related veterinary viruses and need for continued vaccination post measles eradication. Hum. Vaccin Immunother. 2018, 14, 229–233. Takeda, M.; Seki, F.; Yamamoto, Y.; Nao, N.; Tokiwa, H. Animal morbilliviruses and their cross-species transmission potential. Curr. Opin. Virol. 2020, 41, 38–45 Waterhouse, A.; Bertoni, M.; Bienert, S.; Studer, G.; Tauriello, G.; Gumienny, R.; Heer, F.T.; de Beer, T.A.P.; Rempfer, C.; Bordoli, L.; et al. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018, 46, W296–W303 Chattopadhyay, K.; Lazar-Molnar, E.; Yan, Q.; Rubinstein, R.; Zhan, C.; Vigdorovich, V.; Ramagopal, U.A.; Bonanno, J.; Nathenson, S.G.; Almo, S.C. Sequence, structure, function, immunity: Structural genomics of costimulation. Immunol Rev. 2009, 229, 356–386 Yadav, A.K.; Rajak, K.K.; Bhatt, M.; Kumar, A.; Chakravarti, S.; Sankar, M.; Muthuchelvan, D.; Kumar, R.; Khulape, S.; Singh, R.P.; et al. Comparative sequence analysis of morbillivirus receptors and its implication in host range expansion. Can. J. Microbiol. 2019, 65, 783–794 de Vries, R.D.; Ludlow, M.; Verburgh, R.J.; van Amerongen, G.; Yuksel, S.; Nguyen, D.T.; McQuaid, S.; Osterhaus, A.D.; Duprex, W.P.; de Swart, R.L. Measles vaccination of nonhuman primates provides partial protection against infection with canine distemper virus. J. Virol. 2014, 88, 4423–4433. Nambulli, S.; Sharp, C.R.; Acciardo, A.S.; Drexler, J.F.; Duprex, W.P. Mapping the evolutionary trajectories of morbilliviruses: What, where and whither. Curr. Opin. Virol. 2016, 16, 95–105. Otsuki, N.; Sekizuka, T.; Seki, F.; Sakai, K.; Kubota, T.; Nakatsu, Y.; Chen, S.; Fukuhara, H.; Maenaka, K.; Yamaguchi, R.; et al. Canine distemper virus with the intact C protein has the potential to replicate in human epithelial cells by using human nectin4 as a receptor. Virology 2013, 435, 485–492. Uhl, E.W.; Kelderhouse, C.; Buikstra, J.; Blick, J.P.; Bolon, B.; Hogan, R.J. New world origin of canine distemper: Interdisciplinary insights. Int. J. Paleopathol. 2019, 24, 266–278 Sakai, K.; Nagata, N.; Ami, Y.; Seki, F.; Suzaki, Y.; Iwata-Yoshikawa, N.; Suzuki, T.; Fukushi, S.; Mizutani, T.; Yoshikawa, T.; et al. Lethal canine distemper virus outbreak in cynomolgus monkeys in Japan in 2008. J. Virol. 2013, 87, 1105–1114. Yamamoto, Y.; Nakano, S.; Seki, F.; Shigeta, Y.; Ito, S.; Tokiwa, H.; Takeda, M. Computational Analysis Reveals a Critical Point Mutation in the N-Terminal Region of the Signaling Lymphocytic Activation Molecule Responsible for the Cross-Species Infection with Canine Distemper Virus. Molecules 2021, 26, 1262. Seki, F.; Yamamoto, Y.; Fukuhara, H.; Ohishi, K.; Maruyama, T.; Maenaka, K.; Tokiwa, H.; Takeda, M. Measles Virus Hemagglutinin Protein Establishes a Specific Interaction With the Extreme N-Terminal Region of Human Signaling Lymphocytic Activation Molecule to Enhance Infection. Front. Microbiol. 2020, 11, 1830. Pfeffermann, K.; Dorr, M.; Zirkel, F.; von Messling, V. Morbillivirus Pathogenesis and Virus-Host Interactions. Adv. Virus Res. 2018, 100, 75–98 Reddy, T.; Sansom, M.S. Computational virology: From the inside out. Biochim. Biophys. Acta. 2016, 1858, 1610–1618 Huber, R.G.; Marzinek, J.K.; Holdbrook, D.A.; Bond, P.J. Multiscale molecular dynamics simulation approaches to the structure and dynamics of viruses. Prog. Biophys. Mol. Biol. 2017, 128, 121–132 Behera, A.K.; Chandra, I.; Cherian, S.S. Molecular dynamics simulation of the effects of single (S221P) and double (S221P and K216E) mutations in the hemagglutinin protein of influenza A H5N1 virus: A study on host receptor specificity. J. Biomol. Struct. Dyn. 2016, 34, 2054–2067 Dutta, P.; Botlani, M.; Varma, S. Water dynamics at protein–protein interfaces: Molecular dynamics study of virus–host receptor complexes. J. Phys. Chem. B. 2014, 118, 14795–14807 Chan, K.W.; Hsieh, H.H.; Wang, H.C.; Lee, Y.J.; Sung, M.H.; Wong, M.L.; Hsu, W.L. Identification, expression and antigenic analysis of recombinant hemagglutinin proteins of canine distemper virus. J. Virol. Methods. 2009, 155, 18–24 Appel, M.J.; Shek, W.R.; Shesberadaran, H.; Norrby, E. Measles virus and inactivated canine distemper virus induce incomplete immunity to canine distemper. Arch. Virol. 1984, 82, 73–82 Brown, A.L.; Vitamvas, J.A.; Merry, D.L., Jr.; Beckenhauer, W.H. Immune response of pups to modified live-virus canine distemper-measles vaccine. Am. J. Vet. Res. 1972, 33, 1447–1456 Qiu, W.; Zheng, Y.; Zhang, S.; Fan, Q.; Liu, H.; Zhang, F.; Wang, W.; Liao, G.; Hu, R. Canine distemper outbreak in rhesus monkeys, China. Emerg. Infect. Dis. 2011, 17, 1541–1543 Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. Jones, D.T.; Taylor, W.R.; Thornton, J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 1992, 8, 275–282 Sali, A.; Blundell, T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234, 779–815 Zhang, Y.; Skolnick, J. TM-align: A protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 2005, 33, 2302–2309. Berger, J.J.; Barnard, R.J. Effect of diet on fat cell size and hormone-sensitive lipase activity. J. Appl. Physiol. 1999, 87, 227–232 Wiederstein, M.; Sippl, M.J. ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007, 35, W407–W410 Lovell, S.C.; Davis, I.W.; Arendall, W.B., 3rd; de Bakker, P.I.; Word, J.M.; Prisant, M.G.; Richardson, J.S.; Richardson, D.C. Structure validation by Calpha geometry: Phi,psi and Cbeta deviation. Proteins 2003, 50, 437–450 Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2010, 31, 455–461. Vajda, S.; Yueh, C.; Beglov, D.; Bohnuud, T.; Mottarella, S.E.; Xia, B.; Hall, D.R.; Kozakov, D. New additions to the ClusPro server motivated by CAPRI. Proteins 2017, 85, 435–444. Kozakov, D.; Hall, D.R.; Xia, B.; Porter, K.A.; Padhorny, D.; Yueh, C.; Beglov, D.; Vajda, S. The ClusPro web server for protein-protein docking. Nat. Protoc. 2017, 12, 255–278 Barrett, T.; Visser, I.K.; Mamaev, L.; Goatley, L.; van Bressem, M.F.; Osterhaust, A.D. Dolphin and porpoise morbilliviruses are genetically distinct from phocine distemper virus. Virology 1993, 193, 1010–1012. |
| dc.rights.license.none.fl_str_mv |
Atribución – No comercial – Compartir igual |
| dc.rights.accessrights.none.fl_str_mv |
info:eu-repo/semantics/openAccess |
| dc.rights.coar.none.fl_str_mv |
http://purl.org/coar/access_right/c_abf2 |
| rights_invalid_str_mv |
Atribución – No comercial – Compartir igual http://purl.org/coar/access_right/c_abf2 |
| eu_rights_str_mv |
openAccess |
| dc.format.extent.spa.fl_str_mv |
1199 p. |
| dc.coverage.temporal.spa.fl_str_mv |
10 p. |
| dc.publisher.spa.fl_str_mv |
Universidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Medicina Veterinaría y Zootecnia, Bucaramanga MDPI |
| dc.publisher.program.spa.fl_str_mv |
Medicina veterinaria y zootecnia |
| dc.publisher.place.spa.fl_str_mv |
Bucaramanga |
| institution |
Universidad Cooperativa de Colombia |
| bitstream.url.fl_str_mv |
https://repository.ucc.edu.co/bitstreams/4732e8bc-10c9-4f13-bddb-f155b1eec2df/download https://repository.ucc.edu.co/bitstreams/fdb7d73d-09d1-4a5f-9e7f-dcdce6316dae/download https://repository.ucc.edu.co/bitstreams/c1eaca20-5420-4114-905a-023ba897772e/download https://repository.ucc.edu.co/bitstreams/766d13fc-7748-4f55-9658-94c7e6efe87f/download https://repository.ucc.edu.co/bitstreams/80b3d6c7-bbf3-4c61-a8c9-702320faac3c/download https://repository.ucc.edu.co/bitstreams/06216f68-504b-424e-bcf4-b6c5ad21a092/download https://repository.ucc.edu.co/bitstreams/5f144584-40f9-4f5b-a338-25c0ccd709d6/download |
| bitstream.checksum.fl_str_mv |
3bce4f7ab09dfc588f126e1e36e98a45 48c560a4f8cd1a7c6a0aa8448e89972e 82d0c3ad2c7ad82a218a92d43d607a1c 4a5ba155d004b6563cee2a185659708b f55d781eaf952fe42f9a91a5b6fb4266 ed49999b0a74d74dedc5b352bb4845b5 392e9168f7ee2334068cbeee6c4f4a67 |
| bitstream.checksumAlgorithm.fl_str_mv |
MD5 MD5 MD5 MD5 MD5 MD5 MD5 |
| repository.name.fl_str_mv |
Repositorio Institucional Universidad Cooperativa de Colombia |
| repository.mail.fl_str_mv |
bdigital@metabiblioteca.com |
| _version_ |
1811564968525430784 |
| spelling |
Rendón Marín, SantiagoQuintero Gil, CarolinaGuerra, DiegoMuskus, CarlosRuiz Sáenz, Julián 10 p. 2022-02-15T20:17:58Z2022-02-15T20:17:58Z2021-092076-0817doi.org/10.3390/pathogens10091199https://hdl.handle.net/20.500.12494/43971Rendon-Marin, S.; Quintero-Gil, C.; Guerra, D.; Muskus, C.; Ruiz-Saenz, J. Canine Morbillivirus from Colombian Lineage Exhibits In Silico and In Vitro Potential to Infect Human Cells. Pathogens 2021, 10, 1199. https://doi.org/10.3390/pathogens10091199Canine morbillivirus (CDV) is a viral agent that infects domestic dogs and a vast array of wildlife species. It belongs to the Paramyxoviridae family, genus Morbillivirus, which is shared with the Measles virus (MeV). Both viruses employ orthologous cellular receptors, SLAM in mononuclear cells and Nectin-4 in epithelial cells, to enter the cells. Although CDV and MeV hemagglutinin (H) have similar functions in viral pathogenesis and cell tropism, the potential interaction of CDV-H protein with human cellular receptors is still uncertain. Considering that CDV is classified as a multi-host pathogen, the potential risk of CDV transmission to humans has not been fully discarded. In this study, we aimed to evaluate both in silico and in vitro, whether there is a cross-species transmission potential from CDV to humans. To accomplish this, the CDV-H protein belonging to the Colombian lineage was modelled. After model validations, molecular docking and molecular dynamics simulations were carried out between Colombian CDV-H protein and canine and human cellular receptors to determine different aspects of the protein–protein interactions. Moreover, cell lines expressing orthologous cellular receptors, with both reference and wild-type CDV strains, were conducted to determine the CDV cross-species transmission potential from an in vitro model. This in silico and in vitro approach suggests the possibility that CDV interacts with ortholog human SLAM (hSLAM) and human Nectin-4 receptors to infect human cell lines, which could imply a potential cross-species transmission of CDV from dogs to humans.http://scienti.colciencias.gov.co:8081/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0000153095https://orcid.org/0000-0002-1447-1458https://scienti.minciencias.gov.co/gruplac/jsp/visualiza/visualizagr.jsp?nro=00000000000695julian.ruizs@campusucc.edu.cohttps://scholar.google.com/citations?user=o3Y7mZwAAAAJ&hl=es1199 p.Universidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Medicina Veterinaría y Zootecnia, BucaramangaMDPIMedicina veterinaria y zootecniaBucaramangahttps://www.mdpi.com/2076-0817/10/9/1199PathogensMacLachlan, N.; Dubovi, E.; Fenner, F. Fenner’s Veterinary Virology, 4th ed.; Elsevier: Amsterdam, The Netherlands, 2011; pp. 299–325.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.da Fontoura Budaszewski, R.; Streck, A.F.; Nunes Weber, M.; Maboni Siqueira, F.; Muniz Guedes, R.L.; Wageck Canal, C. Influence of vaccine strains on the evolution of canine distemper virus. Infect. Genet. Evol. 2016, 41, 262–269Lamb, R.A.; Parks, G.D. Paramyxoviridae. In Fields Virology, 6th ed.; Wolters Kluwer Health Adis (ESP): Philadelphia, PA, USA, 2013von Messling, V.; Zimmer, G.; Herrler, G.; Haas, L.; Cattaneo, R. The hemagglutinin of canine distemper virus determines tropism and cytopathogenicity. J. Virol. 2001, 75, 6418–6427.von Messling, V.; Oezguen, N.; Zheng, Q.; Vongpunsawad, S.; Braun, W.; Cattaneo, R. Nearby clusters of hemagglutinin residues sustain SLAM-dependent canine distemper virus entry in peripheral blood mononuclear cells. J. Virol. 2005, 79, 5857–5862.Pratakpiriya, W.; Seki, F.; Otsuki, N.; Sakai, K.; Fukuhara, H.; Katamoto, H.; Hirai, T.; Maenaka, K.; Techangamsuwan, S.; Lan, N.T.; et al. Nectin4 is an epithelial cell receptor for canine distemper virus and involved in neurovirulence. J. Virol. 2012, 86, 10207–10210da Fontoura Budaszewski, R.; von Messling, V. Morbillivirus Experimental Animal Models: Measles Virus Pathogenesis Insights from Canine Distemper Virus. Viruses 2016, 8, 274.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.Tatsuo, H.; Ono, N.; Yanagi, Y. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J. Virol. 2001, 75, 5842–5850Rendon-Marin, S.; da Fontoura Budaszewski, R.; Canal, C.W.; Ruiz-Saenz, J. Tropism and molecular pathogenesis of canine distemper virus. Virol. J. 2019, 16, 30.Langedijk, J.P.; Janda, J.; Origgi, F.C.; Orvell, C.; Vandevelde, M.; Zurbriggen, A.; Plattet, P. Canine distemper virus infects canine keratinocytes and immune cells by using overlapping and distinct regions located on one side of the attachment protein. J. Virol. 2011, 85, 11242–11254.Duque-Valencia, J.; Sarute, N.; Olarte-Castillo, X.A.; Ruiz-Saenz, J. Evolution and Interspecies Transmission of Canine Distemper Virus-An Outlook of the Diverse Evolutionary Landscapes of a Multi-Host Virus. Viruses 2019, 11, 582.Mochizuki, M.; Hashimoto, M.; Hagiwara, S.; Yoshida, Y.; Ishiguro, S. Genotypes of canine distemper virus determined by analysis of the hemagglutinin genes of recent isolates from dogs in Japan. J. Clin. Microbiol. 1999, 37, 2936–2942Anis, E.; Newell, T.K.; Dyer, N.; Wilkes, R.P. Phylogenetic analysis of the wild-type strains of canine distemper virus circulating in the United States. Virol. J. 2018, 15, 118Blixenkrone-Moller, M.; Svansson, V.; Appel, M.; Krogsrud, J.; Have, P.; Orvell, C. Antigenic relationships between field isolates of morbilliviruses from different carnivores. Arch. Virol. 1992, 123, 279–294.Espinal, M.A.; Diaz, F.J.; Ruiz-Saenz, J. Phylogenetic evidence of a new canine distemper virus lineage among domestic dogs in Colombia, South America. Vet. Microbiol. 2014, 172, 168–176.Haas, L.; Martens, W.; Greiser-Wilke, I.; Mamaev, L.; Butina, T.; Maack, D.; Barrett, T. Analysis of the haemagglutinin gene of current wild-type canine distemper virus isolates from Germany. Virus Res. 1997, 48, 165–171Harder, T.C.; Kenter, M.; Vos, H.; Siebelink, K.; Huisman, W.; van Amerongen, G.; Orvell, C.; Barrett, T.; Appel, M.J.; Osterhaus, A.D. Canine distemper virus from diseased large felids: Biological properties and phylogenetic relationships. J. Gen. Virol. 1996, 77, 397–405Iwatsuki, K.; Tokiyoshi, S.; Hirayama, N.; Nakamura, K.; Ohashi, K.; Wakasa, C.; Mikami, T.; Kai, C. Antigenic differences in the H proteins of canine distemper viruses. Vet. Microbiol. 2000, 71, 281–286.Panzera, Y.; Calderon, M.G.; Sarute, N.; Guasco, S.; Cardeillac, A.; Bonilla, B.; Hernandez, M.; Francia, L.; Bedo, G.; La Torre, J.; et al. Evidence of two co-circulating genetic lineages of canine distemper virus in South America. Virus Res. 2012, 163, 401–404.Riley, M.C.; Wilkes, R.P. Sequencing of emerging canine distemper virus strain reveals new distinct genetic lineage in the United States associated with disease in wildlife and domestic canine populations. Virol. J. 2015, 12, 219.Nikolin, V.M.; Olarte-Castillo, X.A.; Osterrieder, N.; Hofer, H.; Dubovi, E.; Mazzoni, C.J.; Brunner, E.; Goller, K.V.; Fyumagwa, R.D.; Moehlman, P.D.; et al. Canine distemper virus in the Serengeti ecosystem: Molecular adaptation to different carnivore species. Mol. Ecol. 2017, 26, 2111–2130.Zhao, J.J.; Yan, X.J.; Chai, X.L.; Martella, V.; Luo, G.L.; Zhang, H.L.; Gao, H.; Liu, Y.X.; Bai, X.; Zhang, L.; et al. Phylogenetic analysis of the haemagglutinin gene of canine distemper virus strains detected from breeding foxes, raccoon dogs and minks in China. Vet. Microbiol. 2010, 140, 34–42.Radtanakatikanon, A.; Keawcharoen, J.; Charoenvisal, N.T.; Poovorawan, Y.; Prompetchara, E.; Yamaguchi, R.; Techangamsuwan, S. Genotypic lineages and restriction fragment length polymorphism of canine distemper virus isolates in Thailand. Vet. Microbiol. 2013, 166, 76–83.Duque-Valencia, J.; Forero-Munoz, N.R.; Diaz, F.J.; Martins, E.; Barato, P.; Ruiz-Saenz, J. Phylogenetic evidence of the intercontinental circulation of a Canine distemper virus lineage in the Americas. Sci. Rep. 2019, 9, 15747Duque-Valencia, J.; Diaz, F.J.; Ruiz-Saenz, J. Phylogenomic Analysis of Two Co-Circulating Canine Distemper Virus Lineages in Colombia. Pathogens 2019, 9, 26Ke, G.M.; Ho, C.H.; Chiang, M.J.; Sanno-Duanda, B.; Chung, C.S.; Lin, M.Y.; Shi, Y.Y.; Yang, M.H.; Tyan, Y.C.; Liao, P.C.; et al. Phylodynamic analysis of the canine distemper virus hemagglutinin gene. BMC Vet. Res. 2015, 11, 164Hashiguchi, T.; Ose, T.; Kubota, M.; Maita, N.; Kamishikiryo, J.; Maenaka, K.; Yanagi, Y. Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat. Struct. Mol. Biol. 2011, 18, 135–141.Zhang, X.; Lu, G.; Qi, J.; Li, Y.; He, Y.; Xu, X.; Shi, J.; Zhang, C.W.; Yan, J.; Gao, G.F. Structure of measles virus hemagglutinin bound to its epithelial receptor nectin-4. Nat. Struct. Mol. Biol. 2013, 20, 67–72.Yoshikawa, Y.; Ochikubo, F.; Matsubara, Y.; Tsuruoka, H.; Ishii, M.; Shirota, K.; Nomura, Y.; Sugiyama, M.; Yamanouchi, K. Natural infection with canine distemper virus in a Japanese monkey (Macaca fuscata). Vet. Microbiol. 1989, 20, 193–205.Otsuki, N.; Nakatsu, Y.; Kubota, T.; Sekizuka, T.; Seki, F.; Sakai, K.; Kuroda, M.; Yamaguchi, R.; Takeda, M. The V protein of canine distemper virus is required for virus replication in human epithelial cells. PLoS ONE 2013, 8, e82343Fukuhara, H.; Ito, Y.; Sako, M.; Kajikawa, M.; Yoshida, K.; Seki, F.; Mwaba, M.H.; Hashiguchi, T.; Higashibata, M.A.; Ose, T.; et al. Specificity of Morbillivirus Hemagglutinins to Recognize SLAM of Different Species. Viruses 2019, 11, 761Bieringer, M.; Han, J.W.; Kendl, S.; Khosravi, M.; Plattet, P.; Schneider-Schaulies, J. Experimental adaptation of wild-type canine distemper virus (CDV) to the human entry receptor CD150. PLoS ONE 2013, 8, e57488Krieger, E.; Nabuurs, S.B.; Vriend, G. Homology modeling. Methods Biochem. Anal. 2003, 44, 509–523Quintero-Gil, C.; Rendon-Marin, S.; Martinez-Gutierrez, M.; Ruiz-Saenz, J. Origin of Canine Distemper Virus: Consolidating Evidence to Understand Potential Zoonoses. Front. Microbiol. 2019, 10, 1982.Cosby, S.L.; Weir, L. Measles vaccination: Threat from related veterinary viruses and need for continued vaccination post measles eradication. Hum. Vaccin Immunother. 2018, 14, 229–233.Takeda, M.; Seki, F.; Yamamoto, Y.; Nao, N.; Tokiwa, H. Animal morbilliviruses and their cross-species transmission potential. Curr. Opin. Virol. 2020, 41, 38–45Waterhouse, A.; Bertoni, M.; Bienert, S.; Studer, G.; Tauriello, G.; Gumienny, R.; Heer, F.T.; de Beer, T.A.P.; Rempfer, C.; Bordoli, L.; et al. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018, 46, W296–W303Chattopadhyay, K.; Lazar-Molnar, E.; Yan, Q.; Rubinstein, R.; Zhan, C.; Vigdorovich, V.; Ramagopal, U.A.; Bonanno, J.; Nathenson, S.G.; Almo, S.C. Sequence, structure, function, immunity: Structural genomics of costimulation. Immunol Rev. 2009, 229, 356–386Yadav, A.K.; Rajak, K.K.; Bhatt, M.; Kumar, A.; Chakravarti, S.; Sankar, M.; Muthuchelvan, D.; Kumar, R.; Khulape, S.; Singh, R.P.; et al. Comparative sequence analysis of morbillivirus receptors and its implication in host range expansion. Can. J. Microbiol. 2019, 65, 783–794de Vries, R.D.; Ludlow, M.; Verburgh, R.J.; van Amerongen, G.; Yuksel, S.; Nguyen, D.T.; McQuaid, S.; Osterhaus, A.D.; Duprex, W.P.; de Swart, R.L. Measles vaccination of nonhuman primates provides partial protection against infection with canine distemper virus. J. Virol. 2014, 88, 4423–4433.Nambulli, S.; Sharp, C.R.; Acciardo, A.S.; Drexler, J.F.; Duprex, W.P. Mapping the evolutionary trajectories of morbilliviruses: What, where and whither. Curr. Opin. Virol. 2016, 16, 95–105.Otsuki, N.; Sekizuka, T.; Seki, F.; Sakai, K.; Kubota, T.; Nakatsu, Y.; Chen, S.; Fukuhara, H.; Maenaka, K.; Yamaguchi, R.; et al. Canine distemper virus with the intact C protein has the potential to replicate in human epithelial cells by using human nectin4 as a receptor. Virology 2013, 435, 485–492.Uhl, E.W.; Kelderhouse, C.; Buikstra, J.; Blick, J.P.; Bolon, B.; Hogan, R.J. New world origin of canine distemper: Interdisciplinary insights. Int. J. Paleopathol. 2019, 24, 266–278Sakai, K.; Nagata, N.; Ami, Y.; Seki, F.; Suzaki, Y.; Iwata-Yoshikawa, N.; Suzuki, T.; Fukushi, S.; Mizutani, T.; Yoshikawa, T.; et al. Lethal canine distemper virus outbreak in cynomolgus monkeys in Japan in 2008. J. Virol. 2013, 87, 1105–1114.Yamamoto, Y.; Nakano, S.; Seki, F.; Shigeta, Y.; Ito, S.; Tokiwa, H.; Takeda, M. Computational Analysis Reveals a Critical Point Mutation in the N-Terminal Region of the Signaling Lymphocytic Activation Molecule Responsible for the Cross-Species Infection with Canine Distemper Virus. Molecules 2021, 26, 1262.Seki, F.; Yamamoto, Y.; Fukuhara, H.; Ohishi, K.; Maruyama, T.; Maenaka, K.; Tokiwa, H.; Takeda, M. Measles Virus Hemagglutinin Protein Establishes a Specific Interaction With the Extreme N-Terminal Region of Human Signaling Lymphocytic Activation Molecule to Enhance Infection. Front. Microbiol. 2020, 11, 1830.Pfeffermann, K.; Dorr, M.; Zirkel, F.; von Messling, V. Morbillivirus Pathogenesis and Virus-Host Interactions. Adv. Virus Res. 2018, 100, 75–98Reddy, T.; Sansom, M.S. Computational virology: From the inside out. Biochim. Biophys. Acta. 2016, 1858, 1610–1618Huber, R.G.; Marzinek, J.K.; Holdbrook, D.A.; Bond, P.J. Multiscale molecular dynamics simulation approaches to the structure and dynamics of viruses. Prog. Biophys. Mol. Biol. 2017, 128, 121–132Behera, A.K.; Chandra, I.; Cherian, S.S. Molecular dynamics simulation of the effects of single (S221P) and double (S221P and K216E) mutations in the hemagglutinin protein of influenza A H5N1 virus: A study on host receptor specificity. J. Biomol. Struct. Dyn. 2016, 34, 2054–2067Dutta, P.; Botlani, M.; Varma, S. Water dynamics at protein–protein interfaces: Molecular dynamics study of virus–host receptor complexes. J. Phys. Chem. B. 2014, 118, 14795–14807Chan, K.W.; Hsieh, H.H.; Wang, H.C.; Lee, Y.J.; Sung, M.H.; Wong, M.L.; Hsu, W.L. Identification, expression and antigenic analysis of recombinant hemagglutinin proteins of canine distemper virus. J. Virol. Methods. 2009, 155, 18–24Appel, M.J.; Shek, W.R.; Shesberadaran, H.; Norrby, E. Measles virus and inactivated canine distemper virus induce incomplete immunity to canine distemper. Arch. Virol. 1984, 82, 73–82Brown, A.L.; Vitamvas, J.A.; Merry, D.L., Jr.; Beckenhauer, W.H. Immune response of pups to modified live-virus canine distemper-measles vaccine. Am. J. Vet. Res. 1972, 33, 1447–1456Qiu, W.; Zheng, Y.; Zhang, S.; Fan, Q.; Liu, H.; Zhang, F.; Wang, W.; Liao, G.; Hu, R. Canine distemper outbreak in rhesus monkeys, China. Emerg. Infect. Dis. 2011, 17, 1541–1543Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870–1874.Jones, D.T.; Taylor, W.R.; Thornton, J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 1992, 8, 275–282Sali, A.; Blundell, T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234, 779–815Zhang, Y.; Skolnick, J. TM-align: A protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 2005, 33, 2302–2309.Berger, J.J.; Barnard, R.J. Effect of diet on fat cell size and hormone-sensitive lipase activity. J. Appl. Physiol. 1999, 87, 227–232Wiederstein, M.; Sippl, M.J. ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007, 35, W407–W410Lovell, S.C.; Davis, I.W.; Arendall, W.B., 3rd; de Bakker, P.I.; Word, J.M.; Prisant, M.G.; Richardson, J.S.; Richardson, D.C. Structure validation by Calpha geometry: Phi,psi and Cbeta deviation. Proteins 2003, 50, 437–450Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2010, 31, 455–461.Vajda, S.; Yueh, C.; Beglov, D.; Bohnuud, T.; Mottarella, S.E.; Xia, B.; Hall, D.R.; Kozakov, D. New additions to the ClusPro server motivated by CAPRI. Proteins 2017, 85, 435–444.Kozakov, D.; Hall, D.R.; Xia, B.; Porter, K.A.; Padhorny, D.; Yueh, C.; Beglov, D.; Vajda, S. The ClusPro web server for protein-protein docking. Nat. Protoc. 2017, 12, 255–278Barrett, T.; Visser, I.K.; Mamaev, L.; Goatley, L.; van Bressem, M.F.; Osterhaust, A.D. Dolphin and porpoise morbilliviruses are genetically distinct from phocine distemper virus. Virology 1993, 193, 1010–1012.Canine distemperCellular receptorInter-species transmissionNectin-4SLAM moleculeCanine morbillivirus from colombian lineage exhibits in silico and in vitro potential to infect human cellsArtículos Científicoshttp://purl.org/coar/resource_type/c_2df8fbb1http://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionAtribución – No comercial – Compartir igualinfo:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2PublicationLICENSElicense.txtlicense.txttext/plain; charset=utf-84334https://repository.ucc.edu.co/bitstreams/4732e8bc-10c9-4f13-bddb-f155b1eec2df/download3bce4f7ab09dfc588f126e1e36e98a45MD53ORIGINAL2022_canine_morbillivirus_from_colombian.pdf2022_canine_morbillivirus_from_colombian.pdfapplication/pdf2195662https://repository.ucc.edu.co/bitstreams/fdb7d73d-09d1-4a5f-9e7f-dcdce6316dae/download48c560a4f8cd1a7c6a0aa8448e89972eMD512022_canine_morbillivirus_from_colombian-FormatoLicenciaUso.pdf2022_canine_morbillivirus_from_colombian-FormatoLicenciaUso.pdfapplication/pdf208577https://repository.ucc.edu.co/bitstreams/c1eaca20-5420-4114-905a-023ba897772e/download82d0c3ad2c7ad82a218a92d43d607a1cMD52THUMBNAIL2022_canine_morbillivirus_from_colombian.pdf.jpg2022_canine_morbillivirus_from_colombian.pdf.jpgGenerated Thumbnailimage/jpeg5725https://repository.ucc.edu.co/bitstreams/766d13fc-7748-4f55-9658-94c7e6efe87f/download4a5ba155d004b6563cee2a185659708bMD542022_canine_morbillivirus_from_colombian-FormatoLicenciaUso.pdf.jpg2022_canine_morbillivirus_from_colombian-FormatoLicenciaUso.pdf.jpgGenerated Thumbnailimage/jpeg5445https://repository.ucc.edu.co/bitstreams/80b3d6c7-bbf3-4c61-a8c9-702320faac3c/downloadf55d781eaf952fe42f9a91a5b6fb4266MD55TEXT2022_canine_morbillivirus_from_colombian.pdf.txt2022_canine_morbillivirus_from_colombian.pdf.txtExtracted texttext/plain90227https://repository.ucc.edu.co/bitstreams/06216f68-504b-424e-bcf4-b6c5ad21a092/downloaded49999b0a74d74dedc5b352bb4845b5MD562022_canine_morbillivirus_from_colombian-FormatoLicenciaUso.pdf.txt2022_canine_morbillivirus_from_colombian-FormatoLicenciaUso.pdf.txtExtracted texttext/plain5980https://repository.ucc.edu.co/bitstreams/5f144584-40f9-4f5b-a338-25c0ccd709d6/download392e9168f7ee2334068cbeee6c4f4a67MD5720.500.12494/43971oai:repository.ucc.edu.co:20.500.12494/439712024-08-09 12:27:17.688open.accesshttps://repository.ucc.edu.coRepositorio Institucional Universidad Cooperativa de Colombiabdigital@metabiblioteca.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 |