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mutagenesis on pathology and spread of different viruses should lead to insight into the development of effective antivirals. Understanding and Controlling Host Cytotoxicity. The majority of known biologically active nucleoside analogues have some degree of cytostatic and/or cytotoxic effects. This problem could be caused by a number of factors, most importantly mutagenesis of host cell DNA and gross aberrations of cellular nucleotide pools and metabolism. Developing a greater understanding of cellular nucleotide metabolism may allow development of analogues that exhibit minimal cellular toxicity, yet remain highly mutagenic to viral RNA genomes. Recent work with 20 -substituted nucleosides has been promising in relieving cellular toxicity.57,58 Also of great importance is understanding what, if any, structural characteristics can prevent ribonucleoside analogues from being converted to deoxyribonucleoside analogues in order to prevent incorporation by host DNA polymerases. Understanding the Impact of Resistance. It has become quite clear that resistance to mutagens can occur in virus populations. This observation has brought a number of new questions to the forefront. Most importantly, what effect will the development of resistance have on the pathology and transmission of a particular virus It can be inferred that the ribavirin-resistant phenotypes of HCV and PV are of signi cant lower tness than wild-type virus populations due to the fact that the resistance phenotype quickly gives way to wild-type virus upon cessation of ribavirin exposure. Presumably, resistance is due to enhanced delity of the RdRP, but it is unknown what the effect of this reduction of quasispecies character will have on the virus population. Because these populations are thought to have evolved to exist on the edge of error catastrophe, low- delity replication must be bene cial. It is likely the reduction in variability of the population would affect the ability of a virus to evade the immune defenses of the host, or diminish the ability of the virus to develop further resistance to unrelated antivirals. Further investigation of enhanced- delity riboviruses (such as the ribavirin-resistant variant of poliovirus) in their natural biological context should provide insight into these issues. Lethal mutagens may therefore be a logical addition to drug cocktails, such as those used currently in the treatment of HIV. In fact, Mansky reported an apparent increase in virus mutation frequency during potent antiretroviral therapy (ART).59 Additionally, a high- delity virus may be less likely to infect a new host or even be prevented from replicating throughtout its entire host range.
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Successful antimicrobial strategies have been based on exploiting differences in the biology of host and pathogen. In this chapter, we have explored the strategy of lethal mutagenesis, which targets two important properties of riboviruses: the use of RNA rather than DNA as the genetic material and the error-prone replication of the
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LETHAL MUTAGENESIS: EXPLOITING ERROR-PRONE REPLICATION OF RIBOVIRUSES
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viral genome. Because these characteristics exist in all known RNA viruses, lethal mutagens have potential as broad-spectrum antiviral agents. Recent work with lethal mutagens has resulted in promising advances in understanding the mechanism of lethal mutagenesis as an antiviral strategy. However, there is still much to learn, particularly regarding the effect of mutagenic nucleoside analogues on host processes. Continued study of lethal mutagens and lethal mutagenesis holds great promise for the development of strategies to treat emerging and established RNA virus diseases. ACKNOWLEDGMENTS The authors thank Dr. Nora Chapman and Dr. Steven Tracy (University of Nebraska Medical Center) for providing CVB3/0 cDNA. Data for incorporation of ribavirin by the CVB3/0 polymerase was obtained by Dr. Christian Castro (Pennsylvania State University). Evaluation of ribavirin in Vero 76 cells was performed by Joshua Kucharski (Pennsylvania State University). Research on lethal mutagenesis performed in the Cameron laboratory is funded by grants from the American Heart Association (0340028N) and the National Institutes of Health (AI054776). REFERENCES
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1. Rotz, L. D.; Khan, A. S.; Lillibridge, S. R.; Ostroff, S. M.; Hughes, J. M. Public health assessment of potential biological terrorism agents. Emerging Infect. Dis. 2002, 8, 225 230. 2. Sidwell, R. W.; Huffman, J. H.; Khare, G. P.; Allen, L. B.; Witkowski, J. T.; et al. Broadspectrum antiviral activity of Virazole: 1-beta-D-ribofuranosyl-1,2,4-triazole-3carboxamide. Science 1972, 177, 705 706. 3. Domingo, E.; Escarmis, C.; Sevilla, N.; Moya, A.; Elena, S. F.; et al. Basic concepts in RNA virus evolution. The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance a review. FASEB J. 1996, 10, 859 864. 4. (a) Steinhauer, D. A.; Domingo, E.; Holland, J. J. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 1992, 122, 281 288. (b) Arnold, J. J.; Cameron, C. E. Poliovirus RNA-dependent RNA polymerase (3Dpo1): Presteady-state kinetic analysis of ribonucleotide incorporation in the presence of Mg2 . Biochemistry 2004, 43, 5126 5137. 5. Drake, J. W.; Holland, J. J. Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 13910 13913. 6. Eigen, M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 1971, 58, 465 523. 7. Holmes, E. C. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol. 2003, 11, 543 546. 8. Domingo, E.; Holland, J. J.; Escarmis, C.; Sevilla, N.; Moya, A.; et al. RNA virus mutations and tness for survival. Basic concepts in RNA virus evolution. Annu. Rev. Microbiol. 1997, 51, 151 178.
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