Directed Evolution of Seneca Valley Virus in Tumorsphere and Monolayer Cell Cultures of a Small-Cell Lung Cancer Model
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
3. Results and Discussion
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Liao, J.B. Viruses and human cancer. Yale J. Biol. Med. 2006, 79, 115–122. [Google Scholar] [PubMed]
- Hemminki, O.; Dos Santos, J.M.; Hemminki, A. Oncolytic viruses for cancer immunotherapy. J. Hematol. Oncol. 2020, 13, 84. [Google Scholar] [CrossRef] [PubMed]
- Russell, L.; Peng, K.W.; Russell, S.J.; Diaz, R.M. Oncolytic Viruses: Priming Time for Cancer Immunotherapy. BioDrugs 2019, 33, 485–501. [Google Scholar] [CrossRef]
- Fukuhara, H.; Ino, Y.; Todo, T. Oncolytic virus therapy: A new era of cancer treatment at dawn. Cancer Sci. 2016, 107, 1373–1379. [Google Scholar] [CrossRef] [PubMed]
- Felix, J.; Savvides, S.N. Mechanisms of immunomodulation by mammalian and viral decoy receptors: Insights from structures. Nat. Rev. Immunol. 2017, 17, 112–129. [Google Scholar] [CrossRef]
- Zhang, B.; Cheng, P. Improving antitumor efficacy via combinatorial regimens of oncolytic virotherapy. Mol. Cancer 2020, 19, 158. [Google Scholar] [CrossRef]
- Seegers, S.L.; Frasier, C.; Greene, S.; Nesmelova, I.V.; Grdzelishvili, V.Z. Experimental Evolution Generates Novel Oncolytic Vesicular Stomatitis Viruses with Improved Replication in Virus-Resistant Pancreatic Cancer Cells. J. Virol. 2020, 94, e01643-19. [Google Scholar] [CrossRef]
- Doumayrou, J.; Ryan, M.G.; Wargo, A.R. Method for serial passage of infectious hematopoietic necrosis virus (IHNV) in rainbow trout. Dis. Aquat. Organ. 2019, 134, 223–236. [Google Scholar] [CrossRef]
- Kaufman, H.L.; Kohlhapp, F.J.; Zloza, A. Oncolytic viruses: A new class of immunotherapy drugs. Nat. Rev. Drug. Discov. 2016, 15, 660. [Google Scholar] [CrossRef]
- Fukuhara, H.; Takeshima, Y.; Todo, T. Triple-mutated oncolytic herpes virus for treating both fast- and slow-growing tumors. Cancer Sci. 2021, 112, 3293–3301. [Google Scholar] [CrossRef]
- Cristi, F.; Gutiérrez, T.; Hitt, M.M.; Shmulevitz, M. Genetic Modifications That Expand Oncolytic Virus Potency. Front. Mol. Biosci. 2022, 9, 831091. [Google Scholar] [CrossRef]
- Tian, Y.; Xie, D.; Yang, L. Engineering strategies to enhance oncolytic viruses in cancer immunotherapy. Signal. Transduct. Target. Ther. 2022, 7, 117. [Google Scholar] [CrossRef] [PubMed]
- Presloid, J.B.; Novella, I.S. RNA Viruses and RNAi: Quasispecies Implications for Viral Escape. Viruses 2015, 7, 3226–3240. [Google Scholar] [CrossRef]
- Hicks, A.L.; Duffy, S. Genus-specific substitution rate variability among picornaviruses. J. Virol. 2011, 85, 7942–7947. [Google Scholar] [CrossRef] [PubMed]
- Andino, R.; Domingo, E. Viral quasispecies. Virology 2015, 479–480, 46–51. [Google Scholar] [CrossRef]
- Adeyemi, O.O.; Nicol, C.; Stonehouse, N.J.; Rowlands, D.J. Increasing Type 1 Poliovirus Capsid Stability by Thermal Selection. J. Virol. 2017, 91, e01586-16. [Google Scholar] [CrossRef] [PubMed]
- Elde, N.C. Poliovirus evolution: The strong, silent type. Cell. Host Microbe 2012, 12, 605–606. [Google Scholar] [CrossRef]
- Karakasiliotis, I.; Paximadi, E.; Markoulatos, P. Evolution of a rare vaccine-derived multirecombinant poliovirus. J. Gen. Virol. 2005, 86, 3137–3142. [Google Scholar] [CrossRef]
- Morelli, M.J.; Wright, C.F.; Knowles, N.J.; Juleff, N.; Paton, D.J.; King, D.P.; Haydon, D.T. Evolution of foot-and-mouth disease virus intra-sample sequence diversity during serial transmission in bovine hosts. Vet. Res. 2013, 44, 12. [Google Scholar] [CrossRef]
- Martín-Acebes, M.A.; Vázquez-Calvo, A.; Rincón, V.; Mateu, M.G.; Sobrino, F. A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid resistance. J. Virol. 2011, 85, 2733–2740. [Google Scholar] [CrossRef]
- Liang, T.; Yang, D.; Liu, M.; Sun, C.; Wang, F.; Wang, J.; Wang, H.; Song, S.; Zhou, G.; Yu, L. Selection and characterization of an acid-resistant mutant of serotype O foot-and-mouth disease virus. Arch. Virol. 2014, 159, 657–667. [Google Scholar] [CrossRef] [PubMed]
- Corbett, V.; Hallenbeck, P.; Rychahou, P.; Chauhan, A. Evolving role of seneca valley virus and its biomarker TEM8/ANTXR1 in cancer therapeutics. Front. Mol. Biosci. 2022, 9, 930207. [Google Scholar] [CrossRef] [PubMed]
- Reddy, P.S.; Burroughs, K.D.; Hales, L.M.; Ganesh, S.; Jones, B.H.; Idamakanti, N.; Hay, C.; Li, S.S.; Skele, K.L.; Vasko, A.J.; et al. Seneca Valley virus, a systemically deliverable oncolytic picornavirus, and the treatment of neuroendocrine cancers. J. Natl. Cancer Inst. 2007, 99, 1623–1633. [Google Scholar] [CrossRef]
- Hales, L.M.; Knowles, N.J.; Reddy, P.S.; Xu, L.; Hay, C.; Hallenbeck, P.L. Complete genome sequence analysis of Seneca Valley virus-001, a novel oncolytic picornavirus. J. Gen. Virol. 2008, 89, 1265–1275. [Google Scholar] [CrossRef] [PubMed]
- Strauss, M.; Jayawardena, N.; Sun, E.; Easingwood, R.A.; Burga, L.N.; Bostina, M. Cryo-Electron Microscopy Structure of Seneca Valley Virus Procapsid. J. Virol. 2018, 92, e01927-17. [Google Scholar] [CrossRef] [PubMed]
- Venkataraman, S.; Reddy, S.P.; Loo, J.; Idamakanti, N.; Hallenbeck, P.L.; Reddy, V.S. Structure of Seneca Valley Virus-001: An oncolytic picornavirus representing a new genus. Structure 2008, 16, 1555–1561. [Google Scholar] [CrossRef]
- Miles, L.A.; Burga, L.N.; Gardner, E.E.; Bostina, M.; Poirier, J.T.; Rudin, C.M. Anthrax toxin receptor 1 is the cellular receptor for Seneca Valley virus. J. Clin. Investig. 2017, 127, 2957–2967. [Google Scholar] [CrossRef]
- Jayawardena, N.; Burga, L.N.; Easingwood, R.A.; Takizawa, Y.; Wolf, M.; Bostina, M. Structural basis for anthrax toxin receptor 1 recognition by Seneca Valley Virus. Proc. Natl. Acad. Sci. USA 2018, 115, E10934–E10940. [Google Scholar] [CrossRef]
- Jayawardena, N.; Miles, L.A.; Burga, L.N.; Rudin, C.; Wolf, M.; Poirier, J.T.; Bostina, M. N-Linked Glycosylation on Anthrax Toxin Receptor 1 Is Essential for Seneca Valley Virus Infection. Viruses 2021, 13, 769. [Google Scholar] [CrossRef]
- Pietrzyk, Ł. Biomarkers Discovery for Colorectal Cancer: A Review on Tumor Endothelial Markers as Perspective Candidates. Dis. Markers 2016, 2016, 4912405. [Google Scholar] [CrossRef]
- Shue, Y.T.; Lim, J.S.; Sage, J. Tumor heterogeneity in small cell lung cancer defined and investigated in pre-clinical mouse models. Transl. Lung Cancer Res. 2018, 7, 21–31. [Google Scholar] [CrossRef] [PubMed]
- Groebe, K.; Mueller-Klieser, W. Distributions of oxygen, nutrient, and metabolic waste concentrations in multicellular spheroids and their dependence on spheroid parameters. Eur. Biophys. J. 1991, 19, 169–181. [Google Scholar] [CrossRef] [PubMed]
- Valent, P.; Bonnet, D.; De Maria, R.; Lapidot, T.; Copland, M.; Melo, J.V.; Chomienne, C.; Ishikawa, F.; Schuringa, J.J.; Stassi, G.; et al. Cancer stem cell definitions and terminology: The devil is in the details. Nat. Rev. Cancer 2012, 12, 767–775. [Google Scholar] [CrossRef] [PubMed]
- Weiswald, L.B.; Bellet, D.; Dangles-Marie, V. Spherical cancer models in tumor biology. Neoplasia 2015, 17, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Nunes, A.S.; Barros, A.S.; Costa, E.C.; Moreira, A.F.; Correia, I.J. 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs. Biotechnol. Bioeng. 2019, 116, 206–226. [Google Scholar] [CrossRef]
- Boucherit, N.; Gorvel, L.; Olive, D. 3D Tumor Models and Their Use for the Testing of Immunotherapies. Front. Immunol. 2020, 11, 603640. [Google Scholar] [CrossRef]
- Vitale, C.; Marzagalli, M.; Scaglione, S.; Dondero, A.; Bottino, C.; Castriconi, R. Tumor Microenvironment and Hydrogel-Based 3D Cancer Models for In Vitro Testing Immunotherapies. Cancers 2022, 14, 1013. [Google Scholar] [CrossRef]
- Available online: https://github.com/BioInfoTools/BBMap (accessed on 25 April 2023).
- Available online: https://github.com/BenLangmead/bowtie2 (accessed on 25 April 2023).
- Available online: http://www.htslib.org (accessed on 25 April 2023).
- Wilm, A.; Aw, P.P.; Bertrand, D.; Yeo, G.H.; Ong, S.H.; Wong, C.H.; Khor, C.C.; Petric, R.; Hibberd, M.L.; Nagarajan, N. LoFreq: A sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res. 2012, 40, 11189–11201. [Google Scholar] [CrossRef]
- R Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2014. [Google Scholar]
- Gu, Z.; Gu, L.; Eils, R.; Schlesner, M.; Brors, B. Circlize implements and enhances circular visualization in R. Bioinformatics 2014, 30, 2811–2812. [Google Scholar] [CrossRef]
- Wickham, H. Ggplot2: Elegant Graphics for Data Analysis. Use R! Springer: Berlin/Heidelberg, Germany, 2016. [Google Scholar] [CrossRef]
- Yu, L.; Baxter, P.A.; Zhao, X.; Liu, Z.; Wadhwa, L.; Zhang, Y.; Su, J.M.; Tan, X.; Yang, J.; Adesina, A.; et al. A single intravenous injection of oncolytic picornavirus SVV-001 eliminates medulloblastomas in primary tumor-based orthotopic xenograft mouse models. Neuro Oncol. 2011, 13, 14–27. [Google Scholar] [CrossRef]
- Liu, Z.; Zhao, X.; Mao, H.; Baxter, P.A.; Huang, Y.; Yu, L.; Wadhwa, L.; Su, J.M.; Adesina, A.; Perlaky, L.; et al. Intravenous injection of oncolytic picornavirus SVV-001 prolongs animal survival in a panel of primary tumor-based orthotopic xenograft mouse models of pediatric glioma. Neuro Oncol. 2013, 15, 1173–1185. [Google Scholar] [CrossRef] [PubMed]
- Briones, C.; Domingo, E. Minority report: Hidden memory genomes in HIV-1 quasispecies and possible clinical implications. AIDS Rev. 2008, 10, 93–109. [Google Scholar]
- Ruiz-Jarabo, C.M.; Miller, E.; Gomez-Mariano, G.; Domingo, E. Synchronous loss of quasispecies memory in parallel viral lineages: A deterministic feature of viral quasispecies. J. Mol. Biol. 2003, 333, 553–563. [Google Scholar] [CrossRef] [PubMed]
- Biebricher, C.K.; Eigen, M. The error threshold. Virus Res. 2005, 107, 117–127. [Google Scholar] [CrossRef] [PubMed]
- Domingo, E.; Escarmís, C.; Lázaro, E.; Manrubia, S.C. Quasispecies dynamics and RNA virus extinction. Virus Res. 2005, 107, 129–139. [Google Scholar] [CrossRef]
- Willcocks, M.M.; Locker, N.; Gomwalk, Z.; Royall, E.; Bakhshesh, M.; Belsham, G.J.; Idamakanti, N.; Burroughs, K.D.; Reddy, P.S.; Hallenbeck, P.L.; et al. Structural features of the Seneca Valley virus internal ribosome entry site (IRES) element: A picornavirus with a pestivirus-like IRES. J. Virol. 2011, 85, 4452–4461. [Google Scholar] [CrossRef]
- Lorenz, R.; Bernhart, S.H.; Höner Zu Siederdissen, C.; Tafer, H.; Flamm, C.; Stadler, P.F.; Hofacker, I.L. ViennaRNA Package 2.0. Algorithms Mol. Biol. 2011, 6, 26. [Google Scholar] [CrossRef]
- Zhang, Y.; Wang, J.; Xiao, Y. 3dRNA: Building RNA 3D structure with improved template library. Comput. Struct. Biotechnol. J. 2020, 18, 2416–2423. [Google Scholar] [CrossRef]
- Wang, J.; Wang, J.; Huang, Y.; Xiao, Y. 3dRNA v2.0: An Updated Web Server for RNA 3D Structure Prediction. Int. J. Mol. Sci. 2019, 20, 4116. [Google Scholar] [CrossRef]
- Caspar, D.L.; Klug, A. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 1962, 27, 1–24. [Google Scholar] [CrossRef]
- Gopal, A.; Egecioglu, D.E.; Yoffe, A.M.; Ben-Shaul, A.; Rao, A.L.; Knobler, C.M.; Gelbart, W.M. Viral RNAs are unusually compact. PLoS ONE 2014, 9, e105875. [Google Scholar] [CrossRef] [PubMed]
- Guarné, A.; Tormo, J.; Kirchweger, R.; Pfistermueller, D.; Fita, I.; Skern, T. Structure of the foot-and-mouth disease virus leader protease: A papain-like fold adapted for self-processing and eIF4G recognition. EMBO J. 1998, 17, 7469–7479. [Google Scholar] [CrossRef] [PubMed]
- Gradi, A.; Foeger, N.; Strong, R.; Svitkin, Y.V.; Sonenberg, N.; Skern, T.; Belsham, G.J. Cleavage of eukaryotic translation initiation factor 4GII within foot-and-mouth disease virus-infected cells: Identification of the L-protease cleavage site in vitro. J. Virol. 2004, 78, 3271–3278. [Google Scholar] [CrossRef] [PubMed]
- Nuanualsuwan, S.; Cliver, D.O. Capsid functions of inactivated human picornaviruses and feline calicivirus. Appl. Environ. Microbiol. 2003, 69, 350–357. [Google Scholar] [CrossRef]
- Bostina, M. Monoclonal antibodies point to Achilles’ heel in picornavirus capsid. PLoS Biol. 2019, 17, e3000232. [Google Scholar] [CrossRef]
- Yuan, S.; Li, G.; Wang, Y.; Gao, Q.; Wang, Y.; Cui, R.; Altmeyer, R.; Zou, G. Identification of Positively Charged Residues in Enterovirus 71 Capsid Protein VP1 Essential for Production of Infectious Particles. J. Virol. 2016, 90, 741–752. [Google Scholar] [CrossRef]
- Jun, H.S.; Kang, Y.; Notkins, A.L.; Yoon, J.W. Gain or loss of diabetogenicity resulting from a single point mutation in recombinant encephalomyocarditis virus. J. Virol. 1997, 71, 9782–9785. [Google Scholar] [CrossRef]
- Martinez, M.A.; Dopazo, J.; Hernandez, J.; Mateu, M.G.; Sobrino, F.; Domingo, E.; Knowles, N.J. Evolution of the capsid protein genes of foot-and-mouth disease virus: Antigenic variation without accumulation of amino acid substitutions over six decades. J. Virol. 1992, 66, 3557–3565. [Google Scholar] [CrossRef]
- Liu, F.; Huang, Y.; Wang, Q.; Li, J.; Shan, H. Rescue of Senecavirus A to uncover mutation profiles of its progenies during 80 serial passages in vitro. Vet. Microbiol. 2021, 253, 108969. [Google Scholar] [CrossRef]
- Joshi, L.R.; Mohr, K.A.; Gava, D.; Kutish, G.; Buysse, A.S.; Vannucci, F.A.; Piñeyro, P.E.; Crossley, B.M.; Schiltz, J.J.; Jenkins-Moore, M.; et al. Genetic diversity and evolution of the emerging picornavirus Senecavirus A. J. Gen. Virol. 2020, 101, 175–187. [Google Scholar] [CrossRef]
- Yang, X.; Cheng, A.; Wang, M.; Jia, R.; Sun, K.; Pan, K.; Yang, Q.; Wu, Y.; Zhu, D.; Chen, S.; et al. Structures and Corresponding Functions of Five Types of Picornaviral 2A Proteins. Front. Microbiol. 2017, 8, 1373. [Google Scholar] [CrossRef] [PubMed]
- Carocci, M.; Cordonnier, N.; Huet, H.; Romey, A.; Relmy, A.; Gorna, K.; Blaise-Boisseau, S.; Zientara, S.; Kassimi, L.B. Encephalomyocarditis virus 2A protein is required for viral pathogenesis and inhibition of apoptosis. J. Virol. 2011, 85, 10741–10754. [Google Scholar] [CrossRef] [PubMed]
- Groppo, R.; Palmenberg, A.C. Cardiovirus 2A protein associates with 40S but not 80S ribosome subunits during infection. J. Virol. 2007, 81, 13067–13074. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; Wang, Q.; Huang, Y.; Wang, N.; Shan, H. A 5-Year Review of Senecavirus A in China since Its Emergence in 2015. Front. Vet. Sci. 2020, 7, 567792. [Google Scholar] [CrossRef]
- Xu, W.; Hole, K.; Goolia, M.; Pickering, B.; Salo, T.; Lung, O.; Nfon, C. Genome wide analysis of the evolution of Senecavirus A from swine clinical material and assembly yard environmental samples. PLoS ONE 2017, 12, e0176964. [Google Scholar] [CrossRef]
- Sánchez-Martínez, S.; Madan, V.; Carrasco, L.; Nieva, J.L. Membrane-active peptides derived from picornavirus 2B viroporin. Curr. Protein Pept. Sci. 2012, 13, 632–643. [Google Scholar] [CrossRef]
- Wu, H.; Zhai, X.; Chen, Y.; Wang, R.; Lin, L.; Chen, S.; Wang, T.; Zhong, X.; Wu, X.; Wang, Y.; et al. Protein 2B of Coxsackievirus B3 Induces Autophagy Relying on Its Transmembrane Hydrophobic Sequences. Viruses 2016, 8, 131. [Google Scholar] [CrossRef]
- Ito, M.; Yanagi, Y.; Ichinohe, T. Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLoS Pathog. 2012, 8, e1002857. [Google Scholar] [CrossRef]
- Li, Z.; Zou, Z.; Jiang, Z.; Huang, X.; Liu, Q. Biological Function and Application of Picornaviral 2B Protein: A New Target for Antiviral Drug Development. Viruses 2019, 11, 510. [Google Scholar] [CrossRef]
- De Jong, A.S.; de Mattia, F.; Van Dommelen, M.M.; Lanke, K.; Melchers, W.J.; Willems, P.H.; van Kuppeveld, F.J. Functional analysis of picornavirus 2B proteins: Effects on calcium homeostasis and intracellular protein trafficking. J. Virol. 2008, 82, 3782–3790. [Google Scholar] [CrossRef]
- Xiao, Y.; Dolan, P.T.; Goldstein, E.F.; Li, M.; Farkov, M.; Brodsky, L.; Andino, R. Poliovirus intrahost evolution is required to overcome tissue-specific innate immune responses. Nat. Commun. 2017, 8, 375. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.H.; Gao, Z.L.; Zhang, J.; Ding, Y.Z.; Stipkovits, L.; Szathmary, S.; Pejsak, Z.; Liu, Y.S. The analysis of codon bias of foot-and-mouth disease virus and the adaptation of this virus to the hosts. Infect. Genet. Evol. 2013, 14, 105–110. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.; Li, K.; Chen, W.; Yang, F.; Cao, W.; Zhang, K.; Li, P.; Tang, L.; Zhu, Z.; Zheng, H. Senecavirus A 2B protein suppresses type I interferon production by inducing the degradation of MAVS. Mol. Immunol. 2022, 142, 11–21. [Google Scholar] [CrossRef] [PubMed]
- Wen, W.; Yin, M.; Zhang, H.; Liu, T.; Chen, H.; Qian, P.; Hu, J.; Li, X. Seneca Valley virus 2C and 3C inhibit type I interferon production by inducing the degradation of RIG-I. Virology 2019, 535, 122–129. [Google Scholar] [CrossRef]
- Thurber, G.M.; Zajic, S.C.; Wittrup, K.D. Theoretic criteria for antibody penetration into solid tumors and micrometastases. J. Nucl. Med. 2007, 48, 995–999. [Google Scholar] [CrossRef]
- Liu, T.; Li, X.; Wu, M.; Qin, L.; Chen, H.; Qian, P. Seneca Valley Virus 2C and 3C(pro) Induce Apoptosis via Mitochondrion-Mediated Intrinsic Pathway. Front. Microbiol. 2019, 10, 1202. [Google Scholar] [CrossRef]
- Zell, R. Picornaviridae-the ever-growing virus family. Arch. Virol. 2018, 163, 299–317. [Google Scholar] [CrossRef] [PubMed]
- Jackson, T.; Belsham, G.J. Picornaviruses: A View from 3A. Viruses 2021, 13, 456. [Google Scholar] [CrossRef]
- Wessels, E.; Duijsings, D.; Notebaart, R.A.; Melchers, W.J.; van Kuppeveld, F.J. A proline-rich region in the coxsackievirus 3A protein is required for the protein to inhibit endoplasmic reticulum-to-golgi transport. J. Virol. 2005, 79, 5163–5173. [Google Scholar] [CrossRef]
- Giachetti, C.; Hwang, S.S.; Semler, B.L. cis-acting lesions targeted to the hydrophobic domain of a poliovirus membrane protein involved in RNA replication. J. Virol. 1992, 66, 6045–6057. [Google Scholar] [CrossRef]
- Teterina, N.L.; Rinaudo, M.S.; Ehrenfeld, E. Strand-specific RNA synthesis defects in a poliovirus with a mutation in protein 3A. J. Virol. 2003, 77, 12679–12691. [Google Scholar] [CrossRef] [PubMed]
- Beard, C.W.; Mason, P.W. Genetic determinants of altered virulence of Taiwanese foot-and-mouth disease virus. J. Virol. 2000, 74, 987–991. [Google Scholar] [CrossRef] [PubMed]
- Harris, J.R.; Racaniello, V.R. Amino acid changes in proteins 2B and 3A mediate rhinovirus type 39 growth in mouse cells. J. Virol. 2005, 79, 5363–5373. [Google Scholar] [CrossRef] [PubMed]
- Núñez, J.I.; Baranowski, E.; Molina, N.; Ruiz-Jarabo, C.M.; Sánchez, C.; Domingo, E.; Sobrino, F. A single amino acid substitution in nonstructural protein 3A can mediate adaptation of foot-and-mouth disease virus to the guinea pig. J. Virol. 2001, 75, 3977–3983. [Google Scholar] [CrossRef] [PubMed]
- Arias, A.; Perales, C.; Escarmís, C.; Domingo, E. Deletion mutants of VPg reveal new cytopathology determinants in a picornavirus. PLoS ONE 2010, 5, e10735. [Google Scholar] [CrossRef] [PubMed]
- Spear, A.; Ogram, S.A.; Morasco, B.J.; Smerage, L.E.; Flanegan, J.B. Viral precursor protein P3 and its processed products perform discrete and essential functions in the poliovirus RNA replication complex. Virology 2015, 485, 492–501. [Google Scholar] [CrossRef]
- Kusov, Y.Y.; Morace, G.; Probst, C.; Gauss-Müller, V. Interaction of hepatitis A virus (HAV) precursor proteins 3AB and 3ABC with the 5′ and 3′ termini of the HAV RNA. Virus Res. 1997, 51, 151–157. [Google Scholar] [CrossRef]
- Paul, A.V.; Wimmer, E. Initiation of protein-primed picornavirus RNA synthesis. Virus Res. 2015, 206, 12–26. [Google Scholar] [CrossRef]
- Fernandes, M.H.V.; Maggioli, M.F.; Otta, J.; Joshi, L.R.; Lawson, S.; Diel, D.G. Senecavirus A 3C Protease Mediates Host Cell Apoptosis Late in Infection. Front. Immunol. 2019, 10, 363. [Google Scholar] [CrossRef]
- Gong, P.; Kortus, M.G.; Nix, J.C.; Davis, R.E.; Peersen, O.B. Structures of coxsackievirus, rhinovirus, and poliovirus polymerase elongation complexes solved by engineering RNA mediated crystal contacts. PLoS ONE 2013, 8, e60272. [Google Scholar] [CrossRef]
- Campagnola, G.; Weygandt, M.; Scoggin, K.; Peersen, O. Crystal structure of coxsackievirus B3 3Dpol highlights the functional importance of residue 5 in picornavirus polymerases. J. Virol. 2008, 82, 9458–9464. [Google Scholar] [CrossRef] [PubMed]
- Love, R.A.; Maegley, K.A.; Yu, X.; Ferre, R.A.; Lingardo, L.K.; Diehl, W.; Parge, H.E.; Dragovich, P.S.; Fuhrman, S.A. The crystal structure of the RNA-dependent RNA polymerase from human rhinovirus: A dual function target for common cold antiviral therapy. Structure 2004, 12, 1533–1544. [Google Scholar] [CrossRef] [PubMed]
- Ferrer-Orta, C.; Arias, A.; Agudo, R.; Pérez-Luque, R.; Escarmís, C.; Domingo, E.; Verdaguer, N. The structure of a protein primer-polymerase complex in the initiation of genome replication. EMBO J. 2006, 25, 880–888. [Google Scholar] [CrossRef] [PubMed]
- Shen, H.; Sun, H.; Li, G. What is the role of motif D in the nucleotide incorporation catalyzed by the RNA-dependent RNA polymerase from poliovirus? PLoS Comput. Biol. 2012, 8, e1002851. [Google Scholar] [CrossRef] [PubMed]
- Pfeiffer, J.K.; Kirkegaard, K. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc. Natl. Acad. Sci. USA 2003, 100, 7289–7294. [Google Scholar] [CrossRef] [PubMed]
- Agudo, R.; Ferrer-Orta, C.; Arias, A.; de la Higuera, I.; Perales, C.; Pérez-Luque, R.; Verdaguer, N.; Domingo, E. A multi-step process of viral adaptation to a mutagenic nucleoside analogue by modulation of transition types leads to extinction-escape. PLoS Pathog. 2010, 6, e1001072. [Google Scholar] [CrossRef]
- Ferrer-Orta, C.; Sierra, M.; Agudo, R.; de la Higuera, I.; Arias, A.; Pérez-Luque, R.; Escarmís, C.; Domingo, E.; Verdaguer, N. Structure of foot-and-mouth disease virus mutant polymerases with reduced sensitivity to ribavirin. J. Virol. 2010, 84, 6188–6199. [Google Scholar] [CrossRef]
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Waqqar, S.; Lee, K.; Lawley, B.; Bilton, T.; Quiñones-Mateu, M.E.; Bostina, M.; Burga, L.N. Directed Evolution of Seneca Valley Virus in Tumorsphere and Monolayer Cell Cultures of a Small-Cell Lung Cancer Model. Cancers 2023, 15, 2541. https://doi.org/10.3390/cancers15092541
Waqqar S, Lee K, Lawley B, Bilton T, Quiñones-Mateu ME, Bostina M, Burga LN. Directed Evolution of Seneca Valley Virus in Tumorsphere and Monolayer Cell Cultures of a Small-Cell Lung Cancer Model. Cancers. 2023; 15(9):2541. https://doi.org/10.3390/cancers15092541
Chicago/Turabian StyleWaqqar, Shakeel, Kai Lee, Blair Lawley, Timothy Bilton, Miguel E. Quiñones-Mateu, Mihnea Bostina, and Laura N. Burga. 2023. "Directed Evolution of Seneca Valley Virus in Tumorsphere and Monolayer Cell Cultures of a Small-Cell Lung Cancer Model" Cancers 15, no. 9: 2541. https://doi.org/10.3390/cancers15092541
APA StyleWaqqar, S., Lee, K., Lawley, B., Bilton, T., Quiñones-Mateu, M. E., Bostina, M., & Burga, L. N. (2023). Directed Evolution of Seneca Valley Virus in Tumorsphere and Monolayer Cell Cultures of a Small-Cell Lung Cancer Model. Cancers, 15(9), 2541. https://doi.org/10.3390/cancers15092541