Timothy Jen Reyes Roxas
ABSTRACT
The African Swine Fever Virus (ASFV) is a highly lethal virus that causes the death of pigs a week after its symptoms begin to manifest; hence, a mortality rate reaching up to 100%. Because of the crucial role of pork as a food preference worldwide, significant economic losses due to ASF outbreaks have been experienced. Despite the severity of this disease, there is still no known treatment that can successfully cure ASF. Recently, the role of the histone-like protein pA104R in the viral replication of ASFV has been unraveled and is gathering the attention of many researchers as a potential target to inhibit ASFV infectivity. However, little is known about the relationship of this protein with its homologs across variants of ASF. Therefore, in this study, we characterized their relationship and highlight conserved and variable regions that allow for the design of effective inhibitors. We acquired the nucleotide sequences of all pA104R homologs through the tBLASTn program. These sequences were subjected to multiple sequence alignment (MSA), and the evolutionary behavior of the sequences was then mapped out. The resulting tree was produced from 91 sequences taken from the NCBI database and contained five distinct clades. The phylogenetic analysis revealed that variants from clades “C” and “E” were highly variable, reflecting higher frequencies of gene mutation compared to the other clades. The alignment and midpoint-rooted phylogenetic tree showed the high conservation of pA104R across variants of ASFV. The variable residues were also determined. From these results, we conclude that drugs and drug-like compounds that can block the protein-DNA binding sites can be administered to afflicted pigs all over the world due to the high conservation of the protein across virulent strains. Thus, pA104R has high potential as a target protein for the inhibition of ASFV replication and spread.
- Haim Ashkenazy, Itamar Sela, Eli Levy Karin, Giddy Landan, and Tal Pupko. 2019. Multiple Sequence Alignment Averaging Improves Phylogeny Reconstruction. Systematic Biology 68, 1 (January 2019), 117–130. DOI:https://doi.org/10.1093/sysbio/syy036Google Scholar
Cross Ref
- Levon Aslanyan, Hranush Avagyan, and Zaven Karalyan. 2020. Whole-genome-based phylogeny of African swine fever virus. Veterinary World 13, 10 (October 2020), 2118–2125. DOI:https://doi.org/10.14202/vetworld.2020.2118-2125Google ScholarCross Ref
- Donatella Bacciu, Massimo Deligios, Giovanna Sanna, Maria Paola Madrau, Maria Luisa Sanna, Silvia Dei Giudici, and Annalisa Oggiano. 2016. Genomic analysis of Sardinian 26544/OG10 isolate of African swine fever virus. Virology Reports 6, (2016), 81–89. DOI:https://doi.org/10.1016/j.virep.2016.09.001Google Scholar
- A. D. S. Bastos, M.-L. Penrith, C. Crucière, J. L. Edrich, G. Hutchings, F. Roger, E. Couacy-Hymann, and G. R.Thomson. 2003. Genotyping field strains of African swine fever virus by partial p72 gene characterisation. Archives of Virology 148, 4 (March 2003). DOI:https://doi.org/10.1007/s00705-002-0946-8Google ScholarCross Ref
- Andreas D Baxevanis and David Landsman. 1996. Histone Sequence Database: A Compilation of Highly-Conserved Nucleoprotein Sequences. Nucleic Acids Research 24, 1 (January 1996), 245–247. DOI:https://doi.org/10.1093/nar/24.1.245Google ScholarCross Ref
- Dassault Systèmes BIOVIA. 2021. BIOVIA Discovery Studio.Google Scholar
- Richard P Bishop, Clare Fleischauer, Etienne P de Villiers, Edward A Okoth, Marisa Arias, Carmina Gallardo, and Chris Upton. 2015. Comparative analysis of the complete genome sequences of Kenyan African swine fever virus isolates within p72 genotypes IX and X. Virus Genes 50, 2 (2015), 303–309. DOI:https://doi.org/10.1007/s11262-014-1156-7Google ScholarCross Ref
- Patrick N Bisimwa, Juliette R Ongus, Lucilla Steinaa, Espoir B Bisimwa, Edwina Bochere, Eunice M Machuka, Jean-Baka Domelevo Entfellner, Edward Okoth, and Roger Pelle. 2021. The first complete genome sequence of the African swine fever virus genotype X and serogroup 7 isolated in domestic pigs from the Democratic Republic of Congo. Virol J 18, 1 (January 2021), 23. DOI:https://doi.org/10.1186/s12985-021-01497-0Google ScholarCross Ref
- Sandra Blome, Kati Franzke, and Martin Beer. 2020. African swine fever – A review of current knowledge. Virus Research 287, (2020), 198099. DOI:https://doi.org/10.1016/j.virusres.2020.198099Google Scholar
- Sandra Blome, Claudia Gabriel, and Martin Beer. 2014. Modern adjuvants do not enhance the efficacy of an inactivated African swine fever virus vaccine preparation. Vaccine 32, 31 (2014), 3879–3882. DOI:https://doi.org/10.1016/j.vaccine.2014.05.051Google ScholarCross Ref
- Laia Bosch-Camós, Elisabeth López, and Fernando Rodriguez. 2020. African swine fever vaccines: a promising work still in progress. Porcine Health Management 6, 1 (2020), 17. DOI:https://doi.org/10.1186/s40813-020-00154-2Google ScholarCross Ref
- Laia Bosch-Camós, Elisabeth López, and Fernando Rodriguez. 2020. African swine fever vaccines: a promising work still in progress. Porcine Health Manag 6, (July 2020), 17. DOI:https://doi.org/10.1186/s40813-020-00154-2Google Scholar
- David A G Chapman, Alistair C Darby, Melissa da Silva, Chris Upton, Alan D Radford, and Linda K Dixon. 2011. Genomic analysis of highly virulent Georgia 2007/1 isolate of African swine fever virus. Emerg Infect Dis 17, 4 (April 2011), 599–605. DOI:https://doi.org/10.3201/eid1704.101283Google ScholarCross Ref
- David A.G. Chapman, Vasily Tcherepanov, Chris Upton, and Linda K. Dixon. 2008. Comparison of the genome sequences of non-pathogenic and pathogenic African swine fever virus isolates. Journal of General Virology 89, 2 (February 2008), 397–408. DOI:https://doi.org/10.1099/vir.0.83343-0Google ScholarCross Ref
- Christina CHEN, Sharmistha GHOSH, and Anne GROVE. 2004. Substrate specificity of Helicobacter pylori histone-like HU protein is determined by insufficient stabilization of DNA flexure points. Biochemical Journal 383, 2 (October 2004), 343–351. DOI:https://doi.org/10.1042/BJ20040938Google Scholar
- Xiao-Lin Chu, Bo-Wen Zhang, Quan-Guo Zhang, Bi-Ru Zhu, Kui Lin, and Da-Yong Zhang. 2018. Temperature responses of mutation rate and mutational spectrum in an Escherichia coli strain and the correlation with metabolic rate. BMC Evol Biol 18, 1 (August 2018), 126. DOI:https://doi.org/10.1186/s12862-018-1252-8Google ScholarCross Ref
- Maria Luisa Danzetta, Maria Luisa Marenzoni, Simona Iannetti, Paolo Tizzani, Paolo Calistri, and Francesco Feliziani. 2020. African swine fever: Lessons to learn from past eradication experiences. A systematic review. Frontiers in Veterinary Science 7, (2020). DOI:https://doi.org/10.3389/fvets.2020.00296Google Scholar
- Robert C Edgar. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 1 (2004), 113. DOI:https://doi.org/10.1186/1471-2105-5-113Google ScholarCross Ref
- Robert C Edgar. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 5 (March 2004), 1792–1797. DOI:https://doi.org/10.1093/nar/gkh340Google ScholarCross Ref
- Jan H Forth, Leonie F Forth, Jacqueline King, Oxana Groza, Alexandra Hübner, Ann Sofie Olesen, Dirk Höper, Linda K Dixon, Christopher L Netherton, Thomas Bruun Rasmussen, Sandra Blome, Anne Pohlmann, and Martin Beer. 2019. A Deep-Sequencing Workflow for the Fast and Efficient Generation of High-Quality African Swine Fever Virus Whole-Genome Sequences. Viruses 11, 9 (September 2019), 846. DOI:https://doi.org/10.3390/v11090846Google ScholarCross Ref
- Ferdinando B Freitas, Margarida Simões, Gonçalo Frouco, Carlos Martins, and Fernando Ferreira. 2019. Towards the Generation of an ASFV-pA104R DISC Mutant and a Complementary Cell Line-A Potential Methodology for the Production of a Vaccine Candidate. Vaccines (Basel) 7, 3 (July 2019), 68. DOI:https://doi.org/10.3390/vaccines7030068Google Scholar
- Inmaculada Galindo and Covadonga Alonso. 2017. African swine fever virus: A review. Viruses 9. DOI:https://doi.org/10.3390/v9050103Google Scholar
- C. Gallardo, A. Soler, R. Nieto, C. Cano, V. Pelayo, M. A. Sánchez, G. Pridotkas, J. Fernandez-Pinero, V. Briones, and M. Arias. 2017. Experimental Infection of Domestic Pigs with African Swine Fever Virus Lithuania 2014 Genotype II Field Isolate. Transboundary and Emerging Diseases 64, 1 (February 2017), 300–304. DOI:https://doi.org/10.1111/tbed.12346Google ScholarCross Ref
- Elisabeth Gasteiger, Alexandre Gattiker, Christine Hoogland, Ivan Ivanyi, Ron D Appel, and Amos Bairoch. 2003. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31, 13 (July 2003), 3784–3788. DOI:https://doi.org/10.1093/nar/gkg563Google ScholarCross Ref
- Natasha N Gaudreault, Daniel W Madden, William C Wilson, Jessie D Trujillo, and Juergen A Richt. 2020. African Swine Fever Virus: An Emerging DNA Arbovirus. Frontiers in Veterinary Science 7, (2020), 215. Retrieved from https://www.frontiersin.org/article/10.3389/fvets.2020.00215Google Scholar
- Gautier Gilliaux, Mutien Garigliany, Alain Licoppe, Julien Paternostre, Christophe Lesenfants, Annick Linden, and Daniel Desmecht. 2019. Newly emerged African swine fever virus strain Belgium/Etalle/wb/2018: Complete genomic sequence and comparative analysis with reference p72 genotype II strains. Transboundary and Emerging Diseases 66, 6 (November 2019), 2566–2591. DOI:https://doi.org/10.1111/tbed.13302Google ScholarCross Ref
- Frouco Gonçalo, Freitas Ferdinando B, Coelho João, Leitão Alexandre, Martins Carlos, Ferreira Fernando, and Frueh Klaus. 2021. DNA-Binding Properties of African Swine Fever Virus pA104R, a Histone-Like Protein Involved in Viral Replication and Transcription. Journal of Virology 91, 12 (October 2021), e02498-16. DOI:https://doi.org/10.1128/JVI.02498-16Google Scholar
- Fredrik Granberg, Claudia Torresi, Annalisa Oggiano, Maja Malmberg, Carmen Iscaro, Gian Mario de Mia, and Sándor Belák. 2016. Complete Genome Sequence of an African Swine Fever Virus Isolate from Sardinia, Italy. Genome Announc 4, 6 (November 2016), e01220-16. DOI:https://doi.org/10.1128/genomeA.01220-16Google ScholarCross Ref
- Jaime Huerta-Cepas, François Serra, and Peer Bork. 2016. ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data. Mol Biol Evol 33, 6 (June 2016), 1635–1638. DOI:https://doi.org/10.1093/molbev/msw046Google ScholarCross Ref
- Dmitri Kamashev, Yulia Agapova, Sergey Rastorguev, Anna A. Talyzina, Konstantin M. Boyko, Dmitry A. Korzhenevskiy, Anna Vlaskina, Raif Vasilov, Vladimir I. Timofeev, and Tatiana v. Rakitina. 2017. Comparison of histone-like HU protein DNA-binding properties and HU/IHF protein sequence alignment. PLOS ONE 12, 11 (November 2017), e0188037. DOI:https://doi.org/10.1371/journal.pone.0188037Google ScholarCross Ref
- Ganna Kovalenko, Anne-Lise Ducluzeau, Liudmyla Ishchenko, Mykola Sushko, Maryna Sapachova, Nataliia Rudova, Oleksii Solodiankin, Anton Gerilovych, Ralf Dagdag, Matthew Redlinger, Maksym Bezymennyi, Maciej Frant, Christian E Lange, Inna Dubchak, Andrii A Mezhenskyi, Serhiy Nychyk, Eric Bortz, and Devin M Drown. 2019. Complete Genome Sequence of a Virulent African Swine Fever Virus from a Domestic Pig in Ukraine. Microbiol Resour Announc 8, 42 (October 2019), e00883-19. DOI:https://doi.org/10.1128/MRA.00883-19Google ScholarCross Ref
- T Lewis, L Zsak, T G Burrage, Z Lu, G F Kutish, J G Neilan, and D L Rock. 2000. An African swine fever virus ERV1-ALR homologue, 9GL, affects virion maturation and viral growth in macrophages and viral virulence in swine. J Virol 74, 3 (February 2000), 1275–1285. DOI:https://doi.org/10.1128/jvi.74.3.1275-1285.2000Google ScholarCross Ref
- Ruili Liu, Yeping Sun, Yan Chai, Su Li, Shihua Li, Liang Wang, Jiaqi Su, Shaoxiong Yu, Jinghua Yan, Feng Gao, Gaiping Zhang, Hua-Ji Qiu, George F Gao, Jianxun Qi, and Han Wang. 2020. The structural basis of African swine fever virus pA104R binding to DNA and its inhibition by stilbene derivatives. Proceedings of the National Academy of Sciences 117, 20 (May 2020), 11000. DOI:https://doi.org/10.1073/pnas.1922523117Google Scholar
- Alexander Malogolovkin, Galina Burmakina, Ilya Titov, Alexey Sereda, Andrey Gogin, Elena Baryshnikova, and Denis Kolbasov. 2015. Comparative analysis of african swine fever virus genotypes and serogroups. Emerging Infectious Diseases 21, 2 (2015), 312–315. DOI:https://doi.org/10.3201/eid2102.140649Google ScholarCross Ref
- Alexander Malogolovkin and Denis Kolbasov. 2019. Genetic and antigenic diversity of African swine fever virus. Virus Research 271. DOI:https://doi.org/10.1016/j.virusres.2019.197673Google Scholar
- S A Nadler. 1995. Advantages and disadvantages of molecular phylogenetics: a case study of ascaridoid nematodes. J Nematol 27, 4 (December 1995), 423–432. Retrieved from https://pubmed.ncbi.nlm.nih.gov/19277308Google Scholar
- S Ndlovu, Williamson A.-L., R Malesa, van Heerden J, C I Boshoff, A D S Bastos, L Heath, O Carulei, and Roux Simon. 2022. Genome Sequences of Three African Swine Fever Viruses of Genotypes I, III, and XXII from South Africa and Zambia, Isolated from Ornithodoros Soft Ticks. Microbiology Resource Announcements 9, 10 (April 2022), e01376-19. DOI:https://doi.org/10.1128/MRA.01376-19Google Scholar
- Emma P Njau, Jean-Baka Domelevo Entfellner, Eunice M Machuka, Edwina N Bochere, Sarah Cleaveland, Gabriel M Shirima, Lughano J Kusiluka, Chris Upton, Richard P Bishop, Roger Pelle, and Edward A Okoth. 2021. The first genotype II African swine fever virus isolated in Africa provides insight into the current Eurasian pandemic. Scientific Reports 11, 1 (2021), 13081. DOI:https://doi.org/10.1038/s41598-021-92593-2Google ScholarCross Ref
- Ferenc Olasz, István Mészáros, Szilvia Marton, Győző L Kaján, Vivien Tamás, Gabriella Locsmándi, Tibor Magyar, Ádám Bálint, Krisztián Bányai, and Zoltán Zádori. 2019. A Simple Method for Sample Preparation to Facilitate Efficient Whole-Genome Sequencing of African Swine Fever Virus. Viruses 11, 12 (December 2019), 1129. DOI:https://doi.org/10.3390/v11121129Google ScholarCross Ref
- I C Pan. 1992. African Swine Fever Virus: Generation of Subpopulations with Altered Immunogenicity and Virulence Following Passage in Cell Cultures. Journal of Veterinary Medical Science 54, 1 (1992), 43–52. DOI:https://doi.org/10.1292/jvms.54.43Google ScholarCross Ref
- Muhammad Tariq Pervez, Masroor Ellahi Babar, Asif Nadeem, Muhammad Aslam, Ali Razaawan, Naeem Aslam, Tanveer Hussain, Nasir Naveed, Salman Qadri, Usman Waheed, and Muhammad Shoaib. 2014. Evaluating the accuracy and effciency of multiple sequence alignment methods. Evolutionary Bioinformatics 10, (December 2014), 205–217. DOI:https://doi.org/10.4137/EBo.s19199Google Scholar
- Jonathan Pevsner. 2004. Bioinformatics and Functional Genomics. John Wiley & Sons, Inc., Hoboken, NJ, USA. DOI:https://doi.org/10.1002/047145916XGoogle Scholar
- Morgan N Price, Paramvir S Dehal, and Adam P Arkin. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26, 7 (July 2009), 1641–1650. DOI:https://doi.org/10.1093/molbev/msp077Google ScholarCross Ref
- Ana Luísa Reis, R. M.E. Parkhouse, Ana Raquel Penedos, Carlos Martins, and Alexandre Leitáo. 2007. Systematic analysis of longitudinal serological responses of pigs infected experimentally with African swine fever virus. Journal of General Virology 88, 9 (September 2007), 2426–2434. DOI:https://doi.org/10.1099/vir.0.82857-0Google ScholarCross Ref
- Liu Ruili, Sun Yeping, Chai Yan, Li Su, Li Shihua, Wang Liang, Su Jiaqi, Yu Shaoxiong, Yan Jinghua, Gao Feng, Zhang Gaiping, Qiu Hua-Ji, Gao George F, Qi Jianxun, and Wang Han. 2020. The structural basis of African swine fever virus pA104R binding to DNA and its inhibition by stilbene derivatives. Proceedings of the National Academy of Sciences 117, 20 (May 2020), 11000–11009. DOI:https://doi.org/10.1073/pnas.1922523117Google Scholar
- P J Sánchez-Cordón, M Montoya, A L Reis, and L K Dixon. 2018. African swine fever: A re-emerging viral disease threatening the global pig industry. Vet J 233, (March 2018), 41–48. DOI:https://doi.org/10.1016/j.tvjl.2017.12.025Google ScholarCross Ref
- Hidetoshi Shimodaira. 2002. An Approximately Unbiased Test of Phylogenetic Tree Selection. Systematic Biology 51, 3 (May 2002), 492–508. DOI:https://doi.org/10.1080/10635150290069913Google ScholarCross Ref
- Sun-Young Sunwoo, Daniel Pérez-Núñez, Igor Morozov, Elena G Sánchez, Natasha N Gaudreault, Jessie D Trujillo, Lina Mur, Marisa Nogal, Daniel Madden, Kinga Urbaniak, In Joong Kim, Wenjun Ma, Yolanda Revilla, and Juergen A Richt. 2019. DNA-Protein Vaccination Strategy Does Not Protect from Challenge with African Swine Fever Virus Armenia 2007 Strain. Vaccines (Basel) 7, 1 (January 2019), 12. DOI:https://doi.org/10.3390/vaccines7010012Google Scholar
- Ana Catarina Urbano and Fernando Ferreira. 2020. Role of the DNA-Binding Protein pA104R in ASFV Genome Packaging and as a Novel Target for Vaccine and Drug Development. Vaccines (Basel) 8, 4 (October 2020), 585. DOI:https://doi.org/10.3390/vaccines8040585Google Scholar
- Ana Catarina Urbano and Fernando Ferreira. 2020. Role of the DNA-Binding Protein pA104R in ASFV Genome Packaging and as a Novel Target for Vaccine and Drug Development. Vaccines (Basel) 8, 4 (October 2020), 585. DOI:https://doi.org/10.3390/vaccines8040585Google Scholar
- Tao Wang, Yuan Sun, and Hua Ji Qiu. 2018. African swine fever: An unprecedented disaster and challenge to China. Infectious Diseases of Poverty 7. DOI:https://doi.org/10.1186/s40249-018-0495-3Google Scholar
- Michael Weiß and Markus Göker. 2011. Chapter 12 - Molecular Phylogenetic Reconstruction. In The Yeasts (Fifth Edition), Cletus P Kurtzman, Jack W Fell and Teun Boekhout (eds.). Elsevier, London, 159–174. DOI:https://doi.org/10.1016/B978-0-444-52149-1.00012-4Google Scholar
- Xuexia Wen, Xijun He, Xiang Zhang, Xianfeng Zhang, Liling Liu, Yuntao Guan, Ying Zhang, and Zhigao Bu. 2019. Genome sequences derived from pig and dried blood pig feed samples provide important insights into the transmission of African swine fever virus in China in 2018. Emerg Microbes Infect 8, 1 (2019), 303–306. DOI:https://doi.org/10.1080/22221751.2019.1565915Google ScholarCross Ref
- Marco Wiltgen. 2019. Algorithms for Structure Comparison and Analysis: Homology Modelling of Proteins. In Encyclopedia of Bioinformatics and Computational Biology, Shoba Ranganathan, Michael Gribskov, Kenta Nakai and Christian Schönbach (eds.). Academic Press, Oxford, 38–61. DOI:https://doi.org/10.1016/B978-0-12-809633-8.20484-6Google Scholar
- Dongyan Xiong, Xiaoxu Zhang, Junping Yu, and Hongping Wei. 2019. Rapid phylogenetic analysis of African swine fever virus from metagenomic sequences. bioRxiv (2019). DOI:https://doi.org/10.1101/756726Google Scholar
- Rafael J Yáñez, Javier M Rodrı́guez, Maria L Nogal, Luis Yuste, Carlos Enrı́quez, Jose F Rodriguez, and Eladio Viñuela. 1995. Analysis of the Complete Nucleotide Sequence of African Swine Fever Virus. Virology 208, 1 (1995), 249–278. DOI:https://doi.org/10.1006/viro.1995.1149Google ScholarCross Ref
- L Zsak, M v Borca, G R Risatti, A Zsak, R A French, Z Lu, G F Kutish, J G Neilan, J D Callahan, W M Nelson, and D L Rock. 2005. Preclinical diagnosis of African swine fever in contact-exposed swine by a real-time PCR assay. J Clin Microbiol 43, 1 (January 2005), 112–119. DOI:https://doi.org/10.1128/JCM.43.1.112-119.2005Google ScholarCross Ref
Index Terms
- Phylogenetic Analysis of the Histone-like Protein (pA104R) Reveals High Conservation among African Swine Fever Virus (ASFV) Variants
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