Targeting the Viral Polymerase of Diarrhea-Causing Viruses as a Strategy to Develop a Single Broad-Spectrum Antiviral Therapy
Abstract
:1. Introduction: The Need and the Concept of Antiviral Treatment for Viral Diarrhea
2. The Viral Polymerase as an Antiviral Target
2.1. Functional and Structural Comparison of the Viral Polymerase in Diarrhea-Causing Viruses
2.2. Known Polymerase Inhibitors of Diarrhea-Causing Viruses
2.2.1. Nucleoside Inhibitors
2.2.2. Key Features of an Ideal Broad-Spectrum Nucleoside Inhibitor
2.2.3. Non-Nucleoside Inhibitors
3. Challenges and Potential Limitations to This Approach
3.1. In Vitro and In Vivo Replication Systems Available for Diarrhea-Causing Viruses
3.2 Antiviral Drug Resistance
3.3. Mitochondrial Toxicity
4. Concluding Remarks
Funding
Conflicts of Interest
References
- Tate, J.E.; Burton, A.H.; Boschi-Pinto, C.; Parashar, U.D. Regional, and National Estimates of Rotavirus Mortality in Children <5 Years of Age, 2000-2013. Clin. Infect. Dis. 2016, 62 (Suppl. 2), S96–S105. [Google Scholar] [CrossRef] [PubMed]
- Patel, M.M.; Widdowson, M.A.; Glass, R.I.; Akazawa, K.; Vinjé, J.; Parashar, U.D. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 2008, 14, 1224–1231. [Google Scholar] [CrossRef] [PubMed]
- Vega, E.; Barclay, L.; Gregoricus, N.; Shirley, S.H.; Lee, D.; Vinje, J. Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J. Clin. Microbiol. 2014, 52, 147–155. [Google Scholar] [CrossRef] [PubMed]
- De Clercq, E.; Li, G. Approved Antiviral Drugs over the Past 50 Years. Clin. Microbiol. Rev. 2016, 29, 695–747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Angarone, M.P.; Sheahan, A.; Kamboj, M. Norovirus in Transplantation. Curr. Infect. Dis. Rep. 2016, 18, 17. [Google Scholar] [CrossRef] [PubMed]
- Ruis, C.; Brown, L.K.; Roy, S.; Atkinson, C.; Williams, R.; Burns, S.O.; Yara-Romero, E.; Jacobs, M.; Goldstein, R.; Breuer, J.; et al. Mutagenesis in Norovirus in Response to Favipiravir Treatment. N. Engl. J. Med. 2018, 379, 2173–2176. [Google Scholar] [CrossRef] [PubMed]
- Woodward, J.M.; Gkrania-Klotsas, E.; Cordero-Ng, A.Y.; Aravinthan, A.; Bandoh, B.N.; Liu, H.; Davies, S.; Zhang, H.; Stevenson, P.; Curran, M.D.; et al. The role of chronic norovirus infection in the enteropathy associated with common variable immunodeficiency. Am. J. Gastroenterol. 2015, 110, 320–327. [Google Scholar] [CrossRef] [PubMed]
- CDC. What You Should Know About Flu Antiviral Drugs. Available online: https://www.cdc.gov/flu/antivirals/whatyoushould.htm (accessed on 28 January 2019).
- Ng, K.K.; Arnold, J.J.; Cameron, C.E. Structure-function relationships among RNA-dependent RNA polymerases. Curr. Topics Microbiol. Immunol. 2008, 320, 137–156. [Google Scholar]
- Liu, H.; Naismith, J.H.; Hay, R.T. Adenovirus DNA replication. Curr. Topics Microbiol. Immunol 2003, 272, 131–164. [Google Scholar]
- DeVincenzo, J.P.; McClure, M.W.; Symons, J.A.; Fathi, H.; Westland, C.; Chanda, S.; Lambkin-Williams, R.; Smith, P.; Zhang, Q.; Beigelman, L.; et al. Activity of Oral ALS-008176 in a Respiratory Syncytial Virus Challenge Study. N. Engl. J. Med. 2015, 373, 2048–2058. [Google Scholar] [CrossRef] [PubMed]
- Alam, I.; Lee, J.H.; Cho, K.J.; Han, K.R.; Yang, J.M.; Chung, M.S.; Kim, K.H. Crystal structures of murine norovirus-1 RNA-dependent RNA polymerase in complex with 2-thiouridine or ribavirin. Virology 2012, 426, 143–151. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rohayem, J.; Robel, I.; Jager, K.; Scheffler, U.; Rudolph, W. Protein-primed and de novo initiation of RNA synthesis by norovirus 3Dpol. J. Virol. 2006, 80, 7060–7069. [Google Scholar] [CrossRef] [PubMed]
- Fullerton, S.W.; Blaschke, M.; Coutard, B.; Gebhardt, J.; Gorbalenya, A.; Canard, B.; Tucker, P.A.; Rohayem, J. Structural and functional characterization of sapovirus RNA-dependent RNA polymerase. J. Virol. 2007, 81, 1858–1871. [Google Scholar] [CrossRef] [PubMed]
- Zamyatkin, D.F.; Parra, F.; Alonso, J.M.; Harki, D.A.; Peterson, B.R.; Grochulski, P.; Ng, K.K. Structural insights into mechanisms of catalysis and inhibition in Norwalk virus polymerase. J. Biol. Chem. 2008, 283, 7705–7712. [Google Scholar] [CrossRef] [PubMed]
- Zamyatkin, D.F.; Parra, F.; Machin, A.; Grochulski, P.; Ng, K.K. Binding of 2′-amino-2′-deoxycytidine-5′-triphosphate to norovirus polymerase induces rearrangement of the active site. J. Mol. Biol. 2009, 390, 10–16. [Google Scholar] [CrossRef] [PubMed]
- Zamyatkin, D.; Rao, C.; Hoffarth, E.; Jurca, G.; Rho, H.; Parra, F.; Grochulski, P.; Ng, K.K. Structure of a backtracked state reveals conformational changes similar to the state following nucleotide incorporation in human norovirus polymerase. Acta Crystallogr. D Biol. Crystallogr. 2014, 70, 3099–3109. [Google Scholar] [CrossRef] [PubMed]
- Croci, R.; Pezzullo, M.; Tarantino, D.; Milani, M.; Tsay, S.C.; Sureshbabu, R.; Tsai, Y.J.; Mastrangelo, E.; Rohayem, J.; Bolognesi, M.; et al. Structural bases of norovirus RNA dependent RNA polymerase inhibition by novel suramin-related compounds. PLoS ONE 2014, 9, e91765. [Google Scholar] [CrossRef] [PubMed]
- Mastrangelo, E.; Pezzullo, M.; Tarantino, D.; Petazzi, R.; Germani, F.; Kramer, D.; Robel, I.; Rohayem, J.; Bolognesi, M.; Milani, M. Structure-based inhibition of Norovirus RNA-dependent RNA polymerases. J. Mol. Biol. 2012, 419, 198–210. [Google Scholar] [CrossRef] [PubMed]
- Croci, R.; Tarantino, D.; Milani, M.; Pezzullo, M.; Rohayem, J.; Bolognesi, M.; Mastrangelo, E. PPNDS inhibits murine Norovirus RNA-dependent RNA-polymerase mimicking two RNA stacking bases. FEBS Lett. 2014, 588, 1720–1725. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bruenn, J.A. A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. Nucleic Acids Res. 2003, 31, 1821–1829. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Reilly, E.K.; Kao, C.C. Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure. Virology 1998, 252, 287–303. [Google Scholar] [CrossRef] [PubMed]
- Venkataraman, S.; Prasad, B.; Selvarajan, R. RNA Dependent RNA Polymerases: Insights from Structure, Function and Evolution. Viruses 2018, 10. [Google Scholar] [CrossRef] [PubMed]
- Tarantino, D.; Pezzullo, M.; Mastrangelo, E.; Croci, R.; Rohayem, J.; Robel, I.; Bolognesi, M.; Milani, M. Naphthalene-sulfonate inhibitors of human norovirus RNA-dependent RNA-polymerase. Antiviral. Res. 2014, 102, 23–28. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Butcher, S.J.; Grimes, J.M.; Makeyev, E.V.; Bamford, D.H.; Stuart, D.I. A mechanism for initiating RNA-dependent RNA polymerization. Nature 2001, 410, 235–240. [Google Scholar] [CrossRef] [PubMed]
- Lawton, J.A.; Estes, M.K.; Prasad, B.V. Mechanism of genome transcription in segmented dsRNA viruses. Adv. Virus Res. 2000, 55, 185–229. [Google Scholar] [PubMed]
- Lu, X.; McDonald, S.M.; Tortorici, M.A.; Tao, Y.J.; Vasquez-Del Carpio, R.; Nibert, M.L.; Patton, J.T.; Harrison, S.C. Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1. Structure (London, England : 1993) 2008, 16, 1678–1688. [Google Scholar] [CrossRef] [PubMed]
- Lewis, T.L.; Greenberg, H.B.; Herrmann, J.E.; Smith, L.S.; Matsui, S.M. Analysis of astrovirus serotype 1 RNA, identification of the viral RNA-dependent RNA polymerase motif, and expression of a viral structural protein. J. Virol. 1994, 68, 77–83. [Google Scholar] [PubMed]
- Méndez, E.M.; Velàsquez, R.; Burnham, A.; Arias, C.F. Replication cycle of astroviruses. In Astrovirus Research; Schultz-Cherry, S.E., Ed.; Springer: New York, NY, USA, 2012; pp. 19–45. [Google Scholar]
- Guix, S.; Caballero, S.; Bosch, A.; Pinto, R.M. C-terminal nsP1a protein of human astrovirus colocalizes with the endoplasmic reticulum and viral RNA. J. Virol. 2004, 78, 13627–13636. [Google Scholar] [CrossRef] [PubMed]
- Toh, Y.; Harper, J.; Dryden, K.A.; Yeager, M.; Arias, C.F.; Mendez, E.; Tao, Y.J. Crystal Structure of the Human Astrovirus Capsid Protein. J. Virol. 2016, 90, 9008–9017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- York, R.L.; Yousefi, P.A.; Bogdanoff, W.; Haile, S.; Tripathi, S.; DuBois, R.M. Structural, Mechanistic, and Antigenic Characterization of the Human Astrovirus Capsid. J. Virol. 2015, 90, 2254–2263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dong, J.; Dong, L.; Mendez, E.; Tao, Y. Crystal structure of the human astrovirus capsid spike. Proc. Natl. Acad. Sci. USA 2011, 108, 12681–12686. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bogdanoff, W.A.; Campos, J.; Perez, E.I.; Yin, L.; Alexander, D.L.; DuBois, R.M. Structure of a Human Astrovirus Capsid-Antibody Complex and Mechanistic Insights into Virus Neutralization. J. Virol. 2017, 91. [Google Scholar] [CrossRef] [PubMed]
- Consortium, T.U. UniProt: The universal protein knowledgebase. Nucleic Acids Res. 2018, 46, 2699. [Google Scholar]
- NCBI. Available online: https://blast.ncbi.nlm.nih.gov (accessed on 7 December 2018).
- Protein Data Bank. Available online: www.rcsb.org (accessed on 10 December 2018).
- Molecular Operating Environment (MOE). Available online: http://www.chemcomp.com (accessed on 10 December 2018).
- EMBL-EBI. Available online: www.ebi.ac.uk (accessed on 10 December 2018).
- Dufour, E.; Mendez, J.; Lazaro, J.M.; de Vega, M.; Blanco, L.; Salas, M. An aspartic acid residue in TPR-1, a specific region of protein-priming DNA polymerases, is required for the functional interaction with primer terminal protein. J. Mol. Biol. 2000, 304, 289–300. [Google Scholar] [CrossRef] [PubMed]
- Hoeben, R.C.; Uil, T.G. Adenovirus DNA replication. Cold Spring Harb. Perspect. Biol. 2013, 5, a013003. [Google Scholar] [CrossRef] [PubMed]
- Salas, M. Protein-priming of DNA replication. Annu. Rev. Biochem. 1991, 60, 39–71. [Google Scholar] [CrossRef] [PubMed]
- Berman, A.J.; Kamtekar, S.; Goodman, J.L.; Lazaro, J.M.; de Vega, M.; Blanco, L.; Salas, M.; Steitz, T.A. Structures of phi29 DNA polymerase complexed with substrate: The mechanism of translocation in B-family polymerases. Embo J. 2007, 26, 3494–3505. [Google Scholar] [CrossRef] [PubMed]
- Choi, K.H. Viral polymerases. Adv. Exp. Med. Biol. 2012, 726, 267–304. [Google Scholar] [CrossRef] [PubMed]
- Naccache, S.N.; Peggs, K.S.; Mattes, F.M.; Phadke, R.; Garson, J.A.; Grant, P.; Samayoa, E.; Federman, S.; Miller, S.; Lunn, M.P.; et al. Diagnosis of neuroinvasive astrovirus infection in an immunocompromised adult with encephalitis by unbiased next-generation sequencing. Clin. Infect. Dis. 2015, 60, 919–923. [Google Scholar] [CrossRef] [PubMed]
- Fremond, M.L.; Perot, P.; Muth, E.; Cros, G.; Dumarest, M.; Mahlaoui, N.; Seilhean, D.; Desguerre, I.; Hebert, C.; Corre-Catelin, N.; et al. Next-Generation Sequencing for Diagnosis and Tailored Therapy: A Case Report of Astrovirus-Associated Progressive Encephalitis. J. Pediatric Infect. Dis. Soc. 2015, 4, e53–e57. [Google Scholar] [CrossRef] [PubMed]
- Rohayem, J.; Bergmann, M.; Gebhardt, J.; Gould, E.; Tucker, P.; Mattevi, A.; Unge, T.; Hilgenfeld, R.; Neyts, J. Antiviral strategies to control calicivirus infections. Antiviral Res. 2010, 87, 162–178. [Google Scholar] [CrossRef] [PubMed]
- Sofia, M.J.; Chang, W.; Furman, P.A.; Mosley, R.T.; Ross, B.S. Nucleoside, nucleotide, and non-nucleoside inhibitors of hepatitis C virus NS5B RNA-dependent RNA-polymerase. J. Med. Chem. 2012, 55, 2481–2531. [Google Scholar] [CrossRef] [PubMed]
- Lanier, R.S.D.; Kolawole, A.; Hosmillo, M.; Nayak, K.; Bae, A.; Gurley, S.; Tippin, T.; Colton, H.; Dunn, J.; Mullin, M.; et al. CMX521: A Nucleoside with Pan-Genotypic Activity against Norovirus. In Proceedings of the 31st International Conference on Antiviral Research, Porto, Portugal, 11–15 June 2018. [Google Scholar]
- Chang, K.O.; George, D.W. Interferons and ribavirin effectively inhibit Norwalk virus replication in replicon-bearing cells. J. Virol. 2007, 81, 12111–12118. [Google Scholar] [CrossRef] [PubMed]
- Furuta, Y.; Takahashi, K.; Shiraki, K.; Sakamoto, K.; Smee, D.F.; Barnard, D.L.; Gowen, B.B.; Julander, J.G.; Morrey, J.D. T-705 (favipiravir) and related compounds: Novel broad-spectrum inhibitors of RNA viral infections. Antiviral Res. 2009, 82, 95–102. [Google Scholar] [CrossRef] [PubMed]
- Rocha-Pereira, J.; Jochmans, D.; Dallmeier, K.; Leyssen, P.; Nascimento, M.S.; Neyts, J. Favipiravir (T-705) inhibits in vitro norovirus replication. Biochem. Biophys. Res. Commun. 2012, 424, 777–780. [Google Scholar] [CrossRef] [PubMed]
- Jin, Z.; Tucker, K.; Lin, X.; Kao, C.C.; Shaw, K.; Tan, H.; Symons, J.; Behera, I.; Rajwanshi, V.K.; Dyatkina, N.; et al. Biochemical Evaluation of the Inhibition Properties of Favipiravir and 2′-C-Methyl-Cytidine Triphosphates against Human and Mouse Norovirus RNA Polymerases. Antimicrob. Agents Chemother. 2015, 59, 7504–7516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arias, A.; Thorne, L.; Goodfellow, I. Favipiravir elicits antiviral mutagenesis during virus replication in vivo. Elife 2014, 3, e03679. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rocha-Pereira, J.; Van Dycke, J.; Neyts, J. Treatment with a Nucleoside Polymerase Inhibitor Reduces Shedding of Murine Norovirus in Stool to Undetectable Levels without Emergence of Drug-Resistant Variants. Antimicrob. Agents Chemother. 2015, 60, 1907–1911. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rocha-Pereira, J.; Jochmans, D.; Dallmeier, K.; Leyssen, P.; Cunha, R.; Costa, I.; Nascimento, M.S.; Neyts, J. Inhibition of norovirus replication by the nucleoside analogue 2′-C-methylcytidine. Biochem. Biophys. Res. Commun. 2012, 427, 796–800. [Google Scholar] [CrossRef] [PubMed]
- Kolawole, A.O.; Rocha-Pereira, J.; Elftman, M.D.; Neyts, J.; Wobus, C.E. Inhibition of human norovirus by a viral polymerase inhibitor in the B cell culture system and in the mouse model. Antiviral Res. 2016, 132, 46–49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Costantini, V.P.; Whitaker, T.; Barclay, L.; Lee, D.; McBrayer, T.R.; Schinazi, R.F.; Vinjé, J. Antiviral activity of nucleoside analogues against norovirus. Antivir. Ther. 2012, 17, 981–991. [Google Scholar] [CrossRef] [PubMed]
- Van Dycke, J.; Arnoldi, F.; Papa, G.; Vandepoele, J.; Burrone, O.R.; Mastrangelo, E.; Tarantino, D.; Heylen, E.; Neyts, J.; Rocha-Pereira, J. A Single Nucleoside Viral Polymerase Inhibitor Against Norovirus, Rotavirus, and Sapovirus-Induced Diarrhea. J. Infect. Dis. 2018, 218, 1753–1758. [Google Scholar] [CrossRef] [PubMed]
- Harki, D.A.; Graci, J.D.; Edathil, J.P.; Castro, C.; Cameron, C.E.; Peterson, B.R. Synthesis of a universal 5-nitroindole ribonucleotide and incorporation into RNA by a viral RNA-dependent RNA polymerase. Chembiochem 2007, 8, 1359–1362. [Google Scholar] [CrossRef] [PubMed]
- Smee, D.F.; Sidwell, R.W.; Clark, S.M.; Barnett, B.B.; Spendlove, R.S. Inhibition of rotaviruses by selected antiviral substances: Mechanisms of viral inhibition and in vivo activity. Antimicrob. Agents Chemother. 1982, 21, 66–73. [Google Scholar] [CrossRef] [PubMed]
- Rios, M.; Munoz, M.; Spencer, E. Antiviral activity of phosphonoformate on rotavirus transcription and replication. Antiviral Res. 1995, 27, 71–83. [Google Scholar] [CrossRef]
- Pizarro, J.M.; Pizarro, J.L.; Fernandez, J.; Sandino, A.M.; Spencer, E. Effect of nucleotide analogues on rotavirus transcription and replication. Virology 1991, 184, 768–772. [Google Scholar] [CrossRef]
- Arnold, A.; MacMahon, E. Adenovirus infections. Medicine 2017, 45, 777–780. [Google Scholar] [CrossRef]
- De Clercq, E. Clinical potential of the acyclic nucleoside phosphonates cidofovir, adefovir, and tenofovir in treatment of DNA virus and retrovirus infections. Clin. Microbiol. Rev. 2003, 16, 569–596. [Google Scholar] [CrossRef] [PubMed]
- Grimley, M.S.; Chemaly, R.F.; Englund, J.A.; Kurtzberg, J.; Chittick, G.; Brundage, T.M.; Bae, A.; Morrison, M.E.; Prasad, V.K. Brincidofovir for Asymptomatic Adenovirus Viremia in Pediatric and Adult Allogeneic Hematopoietic Cell Transplant Recipients: A Randomized Placebo-Controlled Phase II Trial. Biol. Blood Marrow Transplant. 2017, 23, 512–521. [Google Scholar] [CrossRef] [PubMed]
- Baba, M.; Mori, S.; Shigeta, S.; De Clercq, E. Selective inhibitory effect of (S)-9-(3-hydroxy-2-phosphonylmethoxypropyl)adenine and 2'-nor-cyclic GMP on adenovirus replication in vitro. Antimicrob. Agents Chemother. 1987, 31, 337–339. [Google Scholar] [CrossRef] [PubMed]
- Naesens, L.; Lenaerts, L.; Andrei, G.; Snoeck, R.; Van Beers, D.; Holy, A.; Balzarini, J.; De Clercq, E. Antiadenovirus activities of several classes of nucleoside and nucleotide analogues. Antimicrob. Agents. Chemother. 2005, 49, 1010–1016. [Google Scholar] [CrossRef] [PubMed]
- Uckun, F.M.; Pendergrass, S.; Qazi, S.; Samuel, P.; Venkatachalam, T.K. Phenyl phosphoramidate derivatives of stavudine as anti-HIV agents with potent and selective in-vitro antiviral activity against adenovirus. Eur. J. Med. Chem. 2004, 39, 225–234. [Google Scholar] [CrossRef] [PubMed]
- Alexeeva, I.; Dyachenko, N.; Nosach, L.; Zhovnovataya, V.; Rybalko, S.; Lozitskaya, R.; Fedchuk, A.; Lozitsky, V.; Gridina, T.; Shalamay, A.; et al. 6-azacytidine--compound with wide spectrum of antiviral activity. Nucleosides Nucleotides Nucleic Acids 2001, 20, 1147–1152. [Google Scholar] [CrossRef] [PubMed]
- Yates, M.K.; Raje, M.R.; Chatterjee, P.; Spiropoulou, C.F.; Bavari, S.; Flint, M.; Soloveva, V.; Seley-Radtke, K.L. Flex-nucleoside analogues-Novel therapeutics against filoviruses. Bioorg. Med. Chem. Lett. 2017, 27, 2800–2802. [Google Scholar] [CrossRef] [PubMed]
- Mehellou, Y.; Rattan, H.S.; Balzarini, J. The ProTide Prodrug Technology: From the Concept to the Clinic. J. Med. Chem. 2018, 61, 2211–2226. [Google Scholar] [CrossRef] [PubMed]
- Sofia, M.J.; Bao, D.; Chang, W.; Du, J.; Nagarathnam, D.; Rachakonda, S.; Reddy, P.G.; Ross, B.S.; Wang, P.; Zhang, H.R.; et al. Discovery of a beta-d-2'-deoxy-2'-alpha-fluoro-2'-beta-C-methyluridine nucleotide prodrug (PSI-7977) for the treatment of hepatitis C virus. J. Med. Chem. 2010, 53, 7202–7218. [Google Scholar] [CrossRef] [PubMed]
- Korb, O.S.T.; Exner, T.E. PLANTS: Application of ant colony optimization to structure-based drug-design. In: Ant colony optimization and swarm intelligence. In Proceedings of the 5th International Workshop, ANTD, Brussels, Belgium, 4–7 September 2006; pp. 245–258. [Google Scholar]
- Eltahla, A.A.; Lim, K.L.; Eden, J.S.; Kelly, A.G.; Mackenzie, J.M.; White, P.A. Nonnucleoside inhibitors of norovirus RNA polymerase: Scaffolds for rational drug design. Antimicrob. Agents Chemother. 2014, 58, 3115–3123. [Google Scholar] [CrossRef] [PubMed]
- Campagnola, G.; Gong, P.; Peersen, O.B. High-throughput screening identification of poliovirus RNA-dependent RNA polymerase inhibitors. Antiviral Res. 2011, 91, 241–251. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Netzler, N.E.; Enosi Tuipulotu, D.; Eltahla, A.A.; Lun, J.H.; Ferla, S.; Brancale, A.; Urakova, N.; Frese, M.; Strive, T.; Mackenzie, J.M.; et al. Broad-spectrum non-nucleoside inhibitors for caliciviruses. Antiviral Res. 2017, 146, 65–75. [Google Scholar] [CrossRef] [PubMed]
- Jones, M.K.; Watanabe, M.; Zhu, S.; Graves, C.L.; Keyes, L.R.; Grau, K.R.; Gonzalez-Hernandez, M.B.; Iovine, N.M.; Wobus, C.E.; Vinje, J.; et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 2014, 346, 755–759. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ettayebi, K.; Crawford, S.E.; Murakami, K.; Broughman, J.R.; Karandikar, U.; Tenge, V.R.; Neill, F.H.; Blutt, S.E.; Zeng, X.L.; Qu, L.; et al. Replication of human noroviruses in stem cell-derived human enteroids. Science 2016, 353, 1387–1393. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Flynn, W.T.; Saif, L.J.; Moorhead, P.D. Pathogenesis of porcine enteric calicivirus-like virus in four-day-old gnotobiotic pigs. Am. J. Vet. Res. 1988, 49, 819–825. [Google Scholar] [PubMed]
- Chang, K.O.; Sosnovtsev, S.V.; Belliot, G.; Kim, Y.; Saif, L.J.; Green, K.Y. Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc. Natl. Acad. Sci. USA 2004, 101, 8733–8738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolf, J.L.; Cukor, G.; Blacklow, N.R.; Dambrauskas, R.; Trier, J.S. Susceptibility of mice to rotavirus infection: Effects of age and administration of corticosteroids. Infect. Immune. 1981, 33, 565–574. [Google Scholar]
- Ward, L.A.; Rosen, B.I.; Yuan, L.; Saif, L.J. Pathogenesis of an attenuated and a virulent strain of group A human rotavirus in neonatal gnotobiotic pigs. J. Gen. Virol. 1996, 77 Pt 7, 1431–1441. [Google Scholar] [CrossRef] [Green Version]
- Li, J.T.; Wei, J.; Guo, H.X.; Han, J.B.; Ye, N.; He, H.Y.; Yu, T.T.; Wu, Y.Z. Development of a human rotavirus induced diarrhea model in Chinese mini-pigs. World J. Gastroenterol. 2016, 22, 7135–7145. [Google Scholar] [CrossRef] [PubMed]
- Tiemessen, C.T.; Kidd, A.H. Adenovirus type 40 and 41 growth in vitro: Host range diversity reflected by differences in patterns of DNA replication. J. Virol. 1994, 68, 1239–1244. [Google Scholar] [PubMed]
- Brinker, J.P.; Blacklow, N.R.; Herrmann, J.E. Human astrovirus isolation and propagation in multiple cell lines. Arch. Virol. 2000, 145, 1847–1856. [Google Scholar] [CrossRef] [PubMed]
- Marvin, S.A.; Huerta, C.T.; Sharp, B.; Freiden, P.; Cline, T.D.; Schultz-Cherry, S. Type I Interferon Response Limits Astrovirus Replication and Protects against Increased Barrier Permeability In Vitro and In Vivo. J. Virol. 2016, 90, 1988–1996. [Google Scholar] [CrossRef]
- Koci, M.D.; Moser, L.A.; Kelley, L.A.; Larsen, D.; Brown, C.C.; Schultz-Cherry, S. Astrovirus induces diarrhea in the absence of inflammation and cell death. J. Virol. 2003, 77, 11798–11808. [Google Scholar] [CrossRef]
- Ferla, S.; Netzler, N.E.; Ferla, S.; Veronese, S.; Tuipulotu, D.E.; Guccione, S.; Brancale, A.; White, P.A.; Bassetto, M. In silico screening for human norovirus antivirals reveals a novel non-nucleoside inhibitor of the viral polymerase. Sci. Rep. 2018, 8, 4129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shen, L.; Peterson, S.; Sedaghat, A.R.; McMahon, M.A.; Callender, M.; Zhang, H.; Zhou, Y.; Pitt, E.; Anderson, K.S.; Acosta, E.P.; et al. Dose-response curve slope sets class-specific limits on inhibitory potential of anti-HIV drugs. Nat. Med. 2008, 14, 762–766. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gentile, I.; Borgia, F.; Zappulo, E.; Buonomo, A.R.; Spera, A.M.; Castaldo, G.; Borgia, G. Efficacy and Safety of Sofosbuvir in the Treatment of Chronic Hepatitis C: The Dawn of a New Era. Rev. Recent Clin. Trials 2014, 9, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Gritsenko, D.; Hughes, G. Ledipasvir/Sofosbuvir (harvoni): Improving options for hepatitis C virus infection. PT 2015, 40, 256–276. [Google Scholar]
- Mason, S.; Devincenzo, J.P.; Toovey, S.; Wu, J.Z.; Whitley, R.J. Comparison of antiviral resistance across acute and chronic viral infections. Antiviral Res. 2018, 158, 103–112. [Google Scholar] [CrossRef] [PubMed]
- Omura, N.; Fujii, H.; Yoshikawa, T.; Yamada, S.; Harada, S.; Inagaki, T.; Shibamura, M.; Takeyama, H.; Saijo, M. Association between sensitivity of viral thymidine kinase-associated acyclovir-resistant herpes simplex virus type 1 and virulence. Virol. J. 2017, 14, 59. [Google Scholar] [CrossRef] [PubMed]
- Lewis, W.; Simpson, J.F.; Meyer, R.R. Cardiac mitochondrial DNA polymerase-gamma is inhibited competitively and noncompetitively by phosphorylated zidovudine. Circ. Res. 1994, 74, 344–348. [Google Scholar] [CrossRef] [PubMed]
- Jin, Z.; Kinkade, A.; Behera, I.; Chaudhuri, S.; Tucker, K.; Dyatkina, N.; Rajwanshi, V.K.; Wang, G.; Jekle, A.; Smith, D.B.; et al. Structure-activity relationship analysis of mitochondrial toxicity caused by antiviral ribonucleoside analogs. Antiviral Res. 2017, 143, 151–161. [Google Scholar] [CrossRef] [PubMed]
- Kakuda, T.N. Pharmacology of nucleoside and nucleotide reverse transcriptase inhibitor-induced mitochondrial toxicity. Clin. Ther. 2000, 22, 685–708. [Google Scholar] [CrossRef]
- Cherry, C.L.; Wesselingh, S.L. Nucleoside analogues and HIV: The combined cost to mitochondria. J. Antimicrob. Chemother. 2003, 51, 1091–1093. [Google Scholar] [CrossRef]
- Brown, N.A. Progress towards improving antiviral therapy for hepatitis C with hepatitis C virus polymerase inhibitors. Part I: Nucleoside analogues. Expert Opin. Investig. Drugs 2009, 18, 709–725. [Google Scholar] [CrossRef] [PubMed]
- Arnold, J.J.; Sharma, S.D.; Feng, J.Y.; Ray, A.S.; Smidansky, E.D.; Kireeva, M.L.; Cho, A.; Perry, J.; Vela, J.E.; Park, Y.; et al. Sensitivity of mitochondrial transcription and resistance of RNA polymerase II dependent nuclear transcription to antiviral ribonucleosides. PLoS Pathog. 2012, 8, e1003030. [Google Scholar] [CrossRef] [PubMed]
- Feng, J.Y.; Xu, Y.; Barauskas, O.; Perry, J.K.; Ahmadyar, S.; Stepan, G.; Yu, H.; Babusis, D.; Park, Y.; McCutcheon, K.; et al. Role of Mitochondrial RNA Polymerase in the Toxicity of Nucleotide Inhibitors of Hepatitis C Virus. Antimicrob. Agents Chemother. 2016, 60, 806–817. [Google Scholar] [CrossRef] [PubMed]
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Bassetto, M.; Van Dycke, J.; Neyts, J.; Brancale, A.; Rocha-Pereira, J. Targeting the Viral Polymerase of Diarrhea-Causing Viruses as a Strategy to Develop a Single Broad-Spectrum Antiviral Therapy. Viruses 2019, 11, 173. https://doi.org/10.3390/v11020173
Bassetto M, Van Dycke J, Neyts J, Brancale A, Rocha-Pereira J. Targeting the Viral Polymerase of Diarrhea-Causing Viruses as a Strategy to Develop a Single Broad-Spectrum Antiviral Therapy. Viruses. 2019; 11(2):173. https://doi.org/10.3390/v11020173
Chicago/Turabian StyleBassetto, Marcella, Jana Van Dycke, Johan Neyts, Andrea Brancale, and Joana Rocha-Pereira. 2019. "Targeting the Viral Polymerase of Diarrhea-Causing Viruses as a Strategy to Develop a Single Broad-Spectrum Antiviral Therapy" Viruses 11, no. 2: 173. https://doi.org/10.3390/v11020173