Replication Kinetics and Infectivity of African Swine Fever Virus (ASFV) Variants with Different Genotypes or Levels of Virulence in Cell Culture Models of Primary Porcine Macrophages
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Viruses and Cells
2.3. Virus Inoculation and Sample Collection
2.4. Real-Time qPCR
2.5. Virus Titration and Detection with Immunoperoxidase Test (IPT)
2.6. Immunofluorescence Microscopy
2.7. Statistical Analysis
3. Results
3.1. Determination of the Purity of the Extracted Cells
3.2. Determination of Intracellular and Extracellular Viral DNA Copy Numbers
3.3. Titration of Infectious Virus in Cells and Extracellular Supernatants
3.4. Percentage of ASFV-Infected Cells
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tulman, E.R.; Delhon, G.A.; Ku, B.K.; Rock, D.L. African Swine Fever Virus. In Lesser Known Large dsDNA Viruses; Van Etten, J.L., Ed.; Springer: Berlin/Heidelberg, Germany, 2009; pp. 43–87. [Google Scholar]
- Licoppe, A.; De Waele, V.; Malengreaux, C.; Paternostre, J.; Van Goethem, A.; Desmecht, D.; Herman, M.; Linden, A. Management of a Focal Introduction of ASF Virus in Wild Boar: The Belgian Experience. Pathogens 2023, 12, 152. [Google Scholar] [CrossRef] [PubMed]
- Sauter-Louis, C.; Conraths, F.J.; Probst, C.; Blohm, U.; Schulz, K.; Sehl, J.; Fischer, M.; Forth, J.H.; Zani, L.; Depner, K.; et al. African Swine Fever in Wild Boar in Europe—A Review. Viruses 2021, 13, 1717. [Google Scholar] [CrossRef]
- Busch, F.; Haumont, C.; Penrith, M.L.; Laddomada, A.; Dietze, K.; Globig, A.; Guberti, V.; Zani, L.; Depner, K. Evidence-Based African Swine Fever Policies: Do We Address Virus and Host Adequately? Front. Vet. Sci. 2021, 8, 637487. [Google Scholar] [CrossRef] [PubMed]
- Qu, H.; Ge, S.; Zhang, Y.; Wu, X.; Wang, Z. A Systematic Review of Genotypes and Serogroups of African Swine Fever Virus. Virus Genes 2022, 58, 77–87. [Google Scholar] [CrossRef]
- Spinard, E.; Dinhobl, M.; Tesler, N.; Birtley, H.; Signore, A.V.; Ambagala, A.; Masembe, C.; Borca, M.V.; Gladue, D.P. A Re-Evaluation of African Swine Fever Genotypes Based on P72 Sequences Reveals the Existence of Only Six Distinct P72 Groups. Viruses 2023, 15, 2246. [Google Scholar] [CrossRef]
- Eustace Montgomery, R. On A Form of Swine Fever Occurring in British East Africa (Kenya Colony). J. Comp. Pathol. Ther. 1921, 34, 159–191. [Google Scholar] [CrossRef]
- Penrith, M.L.; Vosloo, W. Review of African Swine Fever: Transmission, Spread and Control: Review Article. J. S. Afr. Vet. Assoc. 2009, 80, 58–62. [Google Scholar] [CrossRef] [PubMed]
- Sánchez, C. La peste porcine africaine: Nouveaux développements. Rev. Sci. Tech. Off. Int. Epiz. 1982, 1, 1031–1064. [Google Scholar]
- Sánchez-Vizcaíno, J.M.; Mur, L.; Gomez-Villamandos, J.C.; Carrasco, L. An Update on the Epidemiology and Pathology of African Swine Fever. J. Comp. Pathol. 2015, 152, 9–21. [Google Scholar] [CrossRef]
- Mur, L.; Atzeni, M.; Martínez-López, B.; Feliziani, F.; Rolesu, S.; Sanchez-Vizcaino, J.M. Thirty-Five-Year Presence of African Swine Fever in Sardinia: History, Evolution and Risk Factors for Disease Maintenance. Transbound. Emerg. Dis. 2016, 63, e165–e177. [Google Scholar] [CrossRef]
- Costard, S.; Mur, L.; Lubroth, J.; Sanchez-Vizcaino, J.M.; Pfeiffer, D.U. Epidemiology of African Swine Fever Virus. Virus Res. 2013, 173, 191–197. [Google Scholar] [CrossRef]
- Beltran-Alcrudo, D.; Lubroth, J.; Depner, K.; De La Rocque, S. African Swine Fever in the Caucasus. Unpublished Work, 2008. Available online: https://openknowledge.fao.org/server/api/core/bitstreams/155da05d-9c7b-4b5b-8428-3fd782dbdfa2/content (accessed on 20 July 2024).
- Beltran-Alcrudo, D.; Guberti, V.; Simone, L.D.; DeCastro, J.; Rozstalnyy, A.; Dietze, K.; Wainwright, S.; Slingenbergh, J. African Swine Fever Spread in the Russian Federation and the Risk for the Region. Unpublished Work, 2009. Available online: https://asf-referencelab.info/asf/images/ficherosasf/FAO_2009.pdf (accessed on 20 July 2024).
- Oganesyan, A.S. African Swine Fever in the Russian Federation: Spatio-Temporal Analysis and Epidemiological Overview. Virus Res. 2013, 173, 204–211. [Google Scholar] [CrossRef]
- Schulz, K.; Oļševskis, E.; Viltrop, A.; Masiulis, M.; Staubach, C.; Nurmoja, I.; Lamberga, K.; Seržants, M.; Malakauskas, A.; Conraths, F.J.; et al. Eight Years of African Swine Fever in the Baltic States: Epidemiological Reflections. Pathogens 2022, 11, 711. [Google Scholar] [CrossRef]
- Giudici, S.D.; Loi, F.; Ghisu, S.; Angioi, P.P.; Zinellu, S.; Fiori, M.S.; Carusillo, F.; Brundu, D.; Franzoni, G.; Zidda, G.M.; et al. The Long-Jumping of African Swine Fever: First Genotype II Notified in Sardinia, Italy. Viruses 2024, 16, 32. [Google Scholar] [CrossRef] [PubMed]
- Pavone, S.; Iscaro, C.; Dettori, A.; Feliziani, F. African Swine Fever: The State of the Art in Italy. Animals 2023, 13, 2998. [Google Scholar] [CrossRef] [PubMed]
- Zhao, D.; Sun, E.; Huang, L.; Ding, L.; Zhu, Y.; Zhang, J.; Shen, D.; Zhang, X.; Zhang, Z.; Ren, T.; et al. Highly Lethal Genotype I and II Recombinant African Swine Fever Viruses Detected in Pigs. Nat. Commun. 2023, 14, 3096. [Google Scholar] [CrossRef]
- Blome, S.; Gabriel, C.; Beer, M. Pathogenesis of African Swine Fever in Domestic Pigs and European Wild Boar. Virus Res. 2013, 173, 122–130. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Cordón, P.J.; Vidaña, B.; Neimanis, A.; Núñez, A.; Wikström, E.; Gavier-Widén, D. 4. Pathology of African Swine Fever. In Understanding and Combatting African Swine Fever; Iacolina, L., Penrith, M.L., Bellini, S., Chenais, E., Jori, F., Montoya, M., Ståhl, K., Gavier-Widén, D., Eds.; Wageningen Academic Publishers: Wageningen, The Netherlands, 2021; pp. 87–139. [Google Scholar]
- Wculek, S.K.; Dunphy, G.; Heras-Murillo, I.; Mastrangelo, A.; Sancho, D. Metabolism of Tissue Macrophages in Homeostasis and Pathology. Cell. Mol. Immunol. 2022, 19, 384–408. [Google Scholar] [CrossRef] [PubMed]
- Álvarez, B.; Revilla, C.; Poderoso, T.; Ezquerra, A.; Domínguez, J. Porcine Macrophage Markers and Populations: An Update. Cells 2023, 12, 2103. [Google Scholar] [CrossRef]
- Colgrove, G.S.; Haelterman, E.O.; Coggins, L. Pathogenesis of African Swine Fever in Young Pigs. Am. J. Vet. Res. 1969, 30, 1343–1359. [Google Scholar]
- Plowright, W.; Parker, J.; Staple, R.F. The Growth of a Virulent Strain of African Swine Fever Virus in Domestic Pigs. J. Hyg. 1968, 66, 117–134. [Google Scholar] [CrossRef] [PubMed]
- Greig, A. Pathogenesis of African Swine Fever in Pigs Naturally Exposed to the Disease. J. Comp. Pathol. 1972, 82, 73–79. [Google Scholar] [CrossRef]
- Wilkinson, P.J.; Donaldson, A.I.; Greig, A.; Bruce, W. Transmission Studies with African Swine Fever Virus: Infections of Pigs by Airborne Virus. J. Comp. Pathol. 1977, 87, 487–495. [Google Scholar] [CrossRef] [PubMed]
- Gómez-Villamandos, J.C.; Bautista, M.J.; Sánchez-Cordón, P.J.; Carrasco, L. Pathology of African Swine Fever: The Role of Monocyte-Macrophage. Virus Res. 2013, 173, 140–149. [Google Scholar] [CrossRef]
- Carrascosa, A.L.; Bustos, M.J.; de Leon, P. Methods for Growing and Titrating African Swine Fever Virus: Field and Laboratory Samples. Curr. Protoc. Cell Biol. 2011, 53, 26.14.1–26.14.25. [Google Scholar] [CrossRef] [PubMed]
- de León, P.; Bustos, M.J.; Carrascosa, A.L. Laboratory Methods to Study African Swine Fever Virus. Virus Res. 2013, 173, 168–179. [Google Scholar] [CrossRef]
- African Swine Fever Virus: Methods and Protocols; Netherton, C.L. (Ed.) Methods in Molecular Biology; Springer: New York, NY, USA, 2022; Volume 2503. [Google Scholar]
- Gao, Y.; Xia, T.; Bai, J.; Zhang, L.; Jiang, X.; Yang, X.; Zhang, K.; Jiang, P. African Swine Fever Virus Exhibits Distinct Replication Defects in Different Cell Types. Viruses 2022, 14, 2642. [Google Scholar] [CrossRef]
- Krug, P.W.; Holinka, L.G.; O’Donnell, V.; Reese, B.; Sanford, B.; Fernandez-Sainz, I.; Gladue, D.P.; Arzt, J.; Rodriguez, L.; Risatti, G.R.; et al. The Progressive Adaptation of a Georgian Isolate of African Swine Fever Virus to Vero Cells Leads to a Gradual Attenuation of Virulence in Swine Corresponding to Major Modifications of the Viral Genome. J. Virol. 2015, 89, 2324–2332. [Google Scholar] [CrossRef] [PubMed]
- Meloni, D.; Franzoni, G.; Oggiano, A. Cell Lines for the Development of African Swine Fever Virus Vaccine Candidates: An Update. Vaccines 2022, 10, 707. [Google Scholar] [CrossRef]
- Borca, M.V.; O’Donnell, V.; Holinka, L.G.; Risatti, G.R.; Ramirez-Medina, E.; Vuono, E.A.; Shi, J.; Pruitt, S.; Rai, A.; Silva, E.; et al. Deletion of CD2-like Gene from the Genome of African Swine Fever Virus Strain Georgia Does Not Attenuate Virulence in Swine. Sci. Rep. 2020, 10, 494. [Google Scholar] [CrossRef]
- Kholod, N.; Koltsov, A.; Krutko, S.; Tulman, E.R.; Namsrayn, S.; Kutish, G.F.; Belov, S.; Korotin, A.; Sukher, M.; Koltsova, G. Comparison of Attenuated and Virulent Strains of African Swine Fever Virus Genotype I and Serogroup 2. Viruses 2023, 15, 1373. [Google Scholar] [CrossRef] [PubMed]
- Franzoni, G.; Graham, S.P.; Giudici, S.D.; Bonelli, P.; Pilo, G.; Anfossi, A.G.; Pittau, M.; Nicolussi, P.S.; Laddomada, A.; Oggiano, A. Characterization of the Interaction of African Swine Fever Virus with Monocytes and Derived Macrophage Subsets. Vet. Microbiol. 2017, 198, 88–98. [Google Scholar] [CrossRef] [PubMed]
- Franzoni, G.; Graham, S.P.; Sanna, G.; Angioi, P.; Fiori, M.S.; Anfossi, A.; Amadori, M.; Dei Giudici, S.; Oggiano, A. Interaction of Porcine Monocyte-Derived Dendritic Cells with African Swine Fever Viruses of Diverse Virulence. Vet. Microbiol. 2018, 216, 190–197. [Google Scholar] [CrossRef] [PubMed]
- Franzoni, G.; Razzuoli, E.; Dei Giudici, S.; Carta, T.; Galleri, G.; Zinellu, S.; Ledda, M.; Angioi, P.; Modesto, P.; Graham, S.P.; et al. Comparison of Macrophage Responses to African Swine Fever Viruses Reveals That the NH/P68 Strain Is Associated with Enhanced Sensitivity to Type I IFN and Cytokine Responses from Classically Activated Macrophages. Pathogens 2020, 9, 209. [Google Scholar] [CrossRef]
- Alkhamis, M.A.; Gallardo, C.; Jurado, C.; Soler, A.; Arias, M. Phylodynamics and Evolutionary Epidemiology of African Swine Fever P72-CVR Genes in Eurasia and Africa. PLoS ONE 2018, 13, e0192565. [Google Scholar]
- Shen, Z.-J.; Jia, H.; Xie, C.-D.; Shagainar, J.; Feng, Z.; Zhang, X.; Li, K.; Zhou, R. Bayesian Phylodynamic Analysis Reveals the Dispersal Patterns of African Swine Fever Virus. Viruses 2022, 14, 889. [Google Scholar] [CrossRef]
- Pikalo, J.; Schoder, M.-E.; Sehl-Ewert, J.; Breithaupt, A.; Cay, A.B.; Lhoëst, C.; van Campe, W.; Mostin, L.; Deutschmann, P.; Roszyk, H.; et al. Towards Efficient Early Warning: Pathobiology of African Swine Fever Virus “Belgium 2018/1” in Domestic Pigs of Different Age Classes. Animals 2021, 11, 2602. [Google Scholar] [CrossRef]
- Linden, A.; Licoppe, A.; Volpe, R.; Paternostre, J.; Lesenfants, C.; Cassart, D.; Garigliany, M.; Tignon, M.; van den Berg, T.; Desmecht, D.; et al. Summer 2018: African Swine Fever Virus Hits North-Western Europe. Transbound. Emerg. Dis. 2019, 66, 54–55. [Google Scholar] [CrossRef]
- Forth, J.H.; Tignon, M.; Cay, A.B.; Forth, L.F.; Höper, D.; Blome, S.; Beer, M. Comparative Analysis of Whole-Genome Sequence of African Swine Fever Virus Belgium 2018/1. Emerg. Infect. Dis. 2019, 25, 1249–1252. [Google Scholar] [CrossRef]
- Gallardo, C.; Nurmoja, I.; Soler, A.; Delicado, V.; Simón, A.; Martin, E.; Perez, C.; Nieto, R.; Arias, M. Evolution in Europe of African Swine Fever Genotype II Viruses from Highly to Moderately Virulent. Vet. Microbiol. 2018, 219, 70–79. [Google Scholar]
- Fernandez, A.; Perez, J.; Carrasco, L.; Sierra, M.A.; Sanchez-Vizcaino, M.; Jover, A. Detection of African Swine Fever Viral Antigens in Paraffin-Embedded Tissues by Use of Immunohistologic Methods and Polyclonal Antibodies. Am. J. Vet. Res. 1992, 53, 1462–1476. [Google Scholar] [CrossRef]
- Leitão, A.; Cartaxeiro, C.; Coelho, R.; Cruz, B.; Parkhouse, R.M.E.; Portugal, F.C.; Vigário, J.D.; Martins, C.L.V. The Non-Haemadsorbing African Swine Fever Virus Isolate ASFV/NH/P68 Provides a Model for Defining the Protective Anti-Virus Immune Response. J. Gen. Virol. 2001, 82, 513–523. [Google Scholar] [CrossRef]
- Berg, C.; Wilker, S.; Roider, J.; Klettner, A. Isolation of Porcine Monocyte Population: A Simple and Efficient Method. Vet. Res. Commun. 2013, 37, 239–241. [Google Scholar] [CrossRef]
- Wensvoort, G.; Terpstra, C.; Pol, J.M.A.; ter Laak, E.A.; Bloemraad, M.; de Kluyver, E.P.; Kragten, C.; van Buiten, L.; den Besten, A.; Wagenaar, F.; et al. Mystery Swine Disease in the Netherlands: The Isolation of Lelystad Virus. Vet. Q. 1991, 13, 121–130. [Google Scholar] [CrossRef]
- Tignon, M.; Gallardo, C.; Iscaro, C.; Hutet, E.; Van der Stede, Y.; Kolbasov, D.; De Mia, G.M.; Le Potier, M.F.; Bishop, R.P.; Arias, M.; et al. Development and Inter-Laboratory Validation Study of an Improved New Real-Time PCR Assay with Internal Control for Detection and Laboratory Diagnosis of African Swine Fever Virus. J. Virol. Methods 2011, 178, 161–170. [Google Scholar] [CrossRef] [PubMed]
- Carmina, G.; Nieto, R.; Arias, M. Indirect Immunoperoxidase Test (IPT) for Detection of Antibodies against African Swine Fever Virus (ASFV) on African Green Monkey Cell Lines (Vero, MS). In African Swine Fever Virus: Methods and Protocols; Netherton, C.L., Ed.; Springer: New York, NY, USA, 2022; pp. 147–158. [Google Scholar]
- Cresta, D.; Warren, D.C.; Quirouette, C.; Smith, A.P.; Lane, L.C.; Smith, A.M.; Beauchemin, C.A.A. Time to Revisit the Endpoint Dilution Assay and to Replace the TCID50 as a Measure of a Virus Sample’s Infection Concentration. PLoS Comput. Biol. 2021, 17, e1009480. [Google Scholar] [CrossRef]
- Sánchez, C.; Gómez-Puertas, P.; Gómez-del-Moral, M.; Alonso, F.; Escribano, J.M.; Ezquerra, A.; Domínguez, J. Expression of Porcine CD163 on Monocytes/Macrophages Correlates with Permissiveness to African Swine Fever Infection. Arch. Virol. 2003, 148, 2307–2323. [Google Scholar] [CrossRef] [PubMed]
- Sánchez, C.; Doménech, N.; Vázquez, J.; Alonso, F.; Ezquerra, A.; Domínguez, J. The Porcine 2A10 Antigen Is Homologous to Human CD163 and Related to Macrophage Differentiation. J. Immunol. 1999, 162, 5230–5237. [Google Scholar] [CrossRef] [PubMed]
- Sánchez, E.G.; Riera, E.; Nogal, M.; Gallardo, C.; Fernández, P.; Bello-Morales, R.; López-Guerrero, J.A.; Chitko-McKown, C.G.; Richt, J.A.; Revilla, Y. Phenotyping and Susceptibility of Established Porcine Cells Lines to African Swine Fever Virus Infection and Viral Production. Sci. Rep. 2017, 7, 10369. [Google Scholar] [CrossRef]
- Vogel, D.Y.S.; Glim, J.E.; Stavenuiter, A.W.D.; Breur, M.; Heijnen, P.; Amor, S.; Dijkstra, C.D.; Beelen, R.H.J. Human Macrophage Polarization in Vitro: Maturation and Activation Methods Compared. Immunobiology 2014, 219, 695–703. [Google Scholar] [CrossRef]
- Carrasco, C.P.; Rigden, R.C.; Schaffner, R.; Gerber, H.; Neuhaus, V.; Inumaru, S.; Takamatsu, H.; Bertoni, G.; McCullough, K.C.; Summerfield, A. Porcine Dendritic Cells Generated in Vitro: Morphological, Phenotypic and Functional Properties. Immunology 2001, 104, 175–184. [Google Scholar] [CrossRef]
- McCullough, K.C.; Basta, S.; Knötig, S.; Gerber, H.; Schaffner, R.; Kim, Y.B.; Saalmüller, A.; Summerfield, A. Intermediate Stages in Monocyte-Macrophage Differentiation Modulate Phenotype and Susceptibility to Virus Infection: Macrophage Differentiation. Immunology 1999, 98, 203–212. [Google Scholar] [CrossRef] [PubMed]
- Duan, X.; Nauwynck, H.J.; Pensaert, M.B. Effects of Origin and State of Differentiation and Activation of Monocytes/Macrophages on Their Susceptibility to Porcine Reproductive and Respiratory Syndrome Virus (PRRSV). Arch. Virol. 1997, 142, 2483–2497. [Google Scholar] [CrossRef] [PubMed]
- Hakizimana, J.N.; Nyabongo, L.; Ntirandekura, J.B.; Yona, C.; Ntakirutimana, D.; Kamana, O.; Nauwynck, H.; Misinzo, G. Genetic Analysis of African Swine Fever Virus From the 2018 Outbreak in South-Eastern Burundi. Front. Vet. Sci. 2020, 7, 578474. [Google Scholar] [CrossRef] [PubMed]
- Wardley, R.C.; Wilkinson, P.J. The Growth of Virulent African Swine Fever Virus in Pig Monocytes and Macrophages. J. Gen. Virol. 1978, 38, 183–186. [Google Scholar] [CrossRef] [PubMed]
- Oh, D.; Han, S.; Tignon, M.; Balmelle, N.; Cay, A.B.; Griffioen, F.; Droesbeke, B.; Nauwynck, H.J. Differential Infection Behavior of African Swine Fever Virus (ASFV) Genotype I and II in the Upper Respiratory Tract. Vet. Res. 2023, 54, 121. [Google Scholar] [CrossRef]
- Howey, E.B. The Pathogenesis of African Swine Fever: Further Characterization of Infection Models and Tissue Dynamics. Doctoral Dissertation, Michigan State University, East Lansing, MI, USA, 2016. [Google Scholar]
- Cai, S.; Zheng, Z.; Cheng, J.; Zhong, L.; Shao, R.; Zheng, F.; Lai, Z.; Ou, J.; Xu, L.; Zhou, P.; et al. Swine Interferon-Inducible Transmembrane Proteins Potently Inhibit African Swine Fever Virus Replication. Front. Immunol. 2022, 13, 827709. [Google Scholar] [CrossRef]
- Fan, W.; Jiao, P.; Zhang, H.; Chen, T.; Zhou, X.; Qi, Y.; Sun, L.; Shang, Y.; Zhu, H.; Hu, R.; et al. Inhibition of African Swine Fever Virus Replication by Porcine Type I and Type II Interferons. Front. Microbiol. 2020, 11, 1203. [Google Scholar] [CrossRef]
- Golding, J.P.; Goatley, L.; Goodbourn, S.; Dixon, L.K.; Taylor, G.; Netherton, C.L. Sensitivity of African Swine Fever Virus to Type I Interferon Is Linked to Genes within Multigene Families 360 and 505. Virology 2016, 493, 154–161. [Google Scholar] [CrossRef]
- McNab, F.; Mayer-Barber, K.; Sher, A.; Wack, A.; O’Garra, A. Type I Interferons in Infectious Disease. Nat. Rev. Immunol. 2015, 15, 87–103. [Google Scholar] [CrossRef]
- Muñoz-Moreno, R.; Cuesta-Geijo, M.Á.; Martínez-Romero, C.; Barrado-Gil, L.; Galindo, I.; García-Sastre, A.; Alonso, C. Antiviral Role of IFITM Proteins in African Swine Fever Virus Infection. PLoS ONE 2016, 11, e0154366. [Google Scholar] [CrossRef] [PubMed]
- Gao, P.; Zhou, L.; Wu, J.; Weng, W.; Wang, H.; Ye, M.; Qu, Y.; Hao, Y.; Zhang, Y.; Ge, X.; et al. Riding Apoptotic Bodies for Cell-Cell Transmission by African Swine Fever Virus. Proc. Natl. Acad. Sci. USA 2023, 120, e2309506120. [Google Scholar] [CrossRef] [PubMed]
- Zsak, L.; Neilan, J.G. Regulation of Apoptosis in African Swine Fever Virus–Infected Macrophages. Sci. World J. 2002, 2, 1186–1195. [Google Scholar] [CrossRef] [PubMed]
- Frydas, I.S.; Nauwynck, H.J. Replication Characteristics of Eight Virulent and Two Attenuated Genotype 1 and 2 Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) Strains in Nasal Mucosa Explants. Vet. Microbiol. 2016, 182, 156–162. [Google Scholar] [CrossRef]
- Frydas, I.S.; Verbeeck, M.; Cao, J.; Nauwynck, H.J. Replication Characteristics of Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) European Subtype 1 (Lelystad) and Subtype 3 (Lena) Strains in Nasal Mucosa and Cells of the Monocytic Lineage: Indications for the Use of New Receptors of PRRSV (Lena). Vet. Res. 2013, 44, 73. [Google Scholar]
- Glorieux, S.; Favoreel, H.W.; Meesen, G.; Van den Broeck, W.; Nauwynck, H.J. Different Replication Characteristics of Historical Pseudorabies Virus Strains in Porcine Respiratory Nasal Mucosa Explants. Vet. Microbiol. 2009, 136, 341–346. [Google Scholar] [CrossRef]
Strain | Origin | Genotype | Virulence | Passage Level on PBMCs | Reference |
---|---|---|---|---|---|
Belgium 2018/01 (BE18) | Belgium, 2018 | II | Virulent | 8 | [43,44] |
Est15/WB-Valga-6 (EST) | Estonia, 2015 | II | Moderately virulent | 3 | [45] |
E70 | Spain, 1970 | I | Virulent | 5 | [46] |
NH/P68 (NHV) | Portugal, 1968 | I | Attenuated | 3 | [47] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Droesbeke, B.; Balmelle, N.; Cay, A.B.; Han, S.; Oh, D.; Nauwynck, H.J.; Tignon, M. Replication Kinetics and Infectivity of African Swine Fever Virus (ASFV) Variants with Different Genotypes or Levels of Virulence in Cell Culture Models of Primary Porcine Macrophages. Microbiol. Res. 2024, 15, 1690-1708. https://doi.org/10.3390/microbiolres15030112
Droesbeke B, Balmelle N, Cay AB, Han S, Oh D, Nauwynck HJ, Tignon M. Replication Kinetics and Infectivity of African Swine Fever Virus (ASFV) Variants with Different Genotypes or Levels of Virulence in Cell Culture Models of Primary Porcine Macrophages. Microbiology Research. 2024; 15(3):1690-1708. https://doi.org/10.3390/microbiolres15030112
Chicago/Turabian StyleDroesbeke, Brecht, Nadège Balmelle, Ann Brigitte Cay, Shaojie Han, Dayoung Oh, Hans J. Nauwynck, and Marylène Tignon. 2024. "Replication Kinetics and Infectivity of African Swine Fever Virus (ASFV) Variants with Different Genotypes or Levels of Virulence in Cell Culture Models of Primary Porcine Macrophages" Microbiology Research 15, no. 3: 1690-1708. https://doi.org/10.3390/microbiolres15030112
APA StyleDroesbeke, B., Balmelle, N., Cay, A. B., Han, S., Oh, D., Nauwynck, H. J., & Tignon, M. (2024). Replication Kinetics and Infectivity of African Swine Fever Virus (ASFV) Variants with Different Genotypes or Levels of Virulence in Cell Culture Models of Primary Porcine Macrophages. Microbiology Research, 15(3), 1690-1708. https://doi.org/10.3390/microbiolres15030112