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Trade-offs in resource allocation in the intracellular life-cycle of hepatitis C virus. (English) Zbl 1414.92134
Summary: Positive sense single-stranded RNA viruses undergo three mutually exclusive processes to replicate within a cell. These are translation to produce proteins, replication to produce RNA viral genomes, and packaging to form virions. The allocation of newly synthesised viral genomes to these processes, which can be regarded as life-history traits, may be subject to natural selection for efficient reproduction. Here, we develop a mathematical model of the process of intracellular viral replication to study alternative strategies for the allocation and reallocation of viral genomes to these processes. We explore four cases of the model: (1) free movement, in which viral genomes can freely be allocated and reallocated among translation, replication and packaging; (2) unidirectional reallocation, in which allocation occurs freely but reallocation can only proceed from translation to replication to packaging; (3) conveyor belt, in which viral genomes are first allocated to translation, then passed on to replication and finally to packaging; and (4) permanent allocation in which new genomes are allocated to the three processes but not reallocated between them. We apply this model to hepatitis C virus and study changes in the production of virus as the rates of allocation and reallocation are varied. We find that high viral production occurs when allocation and reallocation of the genome are weighted towards the translation and replication processes. The replication process in particular is favoured. The most productive strategy is a form of the free movement model in which genomes are allocated entirely to the replication-translation cycle while allowing some genomes to be packaged through reallocation.
MSC:
92C37 Cell biology
92C40 Biochemistry, molecular biology
Software:
deSolve
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[1] Alizon, S.; Hurford, A.; Mideo, N.; Van Baalen, M., Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future, J. evol. biol., 22, 2, 245-259, (2009)
[2] Barclay, W.; Li, Q.; Hutchison, G.; Moon, D.; Richardson, A.; Percy, N.; Almond, J.; Evans, D., Encapsidation studies of poliovirus subgenomic replicons, J. gen. virol., 79, 7, 1725-1734, (1998)
[3] Bull, J.; Pfennig, D.W.; Wang, I.-N., Genetic details, optimization and phage life histories, Trends ecol. evol., 19, 2, 76-82, (2004)
[4] Campbell, N.A.; Reece, J.B.; Meyers, N., Biology, (2006), Benjamin Cummings San Francisco
[5] Coombs, D.; Gilchrist, M.; Ball, C., Evaluating the importance of within- and between-host selection pressures on the evolution of chronic pathogens, Theor. popul. biol., 72, 4, 576-591, (2007) · Zbl 1141.92036
[6] Dahari, H.; Ribeiro, R.M.; Rice, C.M.; Perelson, A.S., Mathematical modeling of subgenomic hepatitis C virus replication in huh-7 cells, J. virol., 81, 2, 750-760, (2007)
[7] Gilchrist, M.A.; Coombs, D.; Perelson, A., Optimizing within-host viral fitness: infected lifespan and virion production rate, J. theor. biol., 229, 2, 281-288, (2004)
[8] Herrmann, E.; Zeuzem, S., The kinetics of hepatitis C virus, Eur. J. gastroenterol. hepatol., 18, 4, 339-342, (2006)
[9] Khromykh, A.; Varnavski, A.; Sedlak, P.; Westaway, E., Coupling between replication and packaging of flavivirus RNA: evidence derived from the use of DNA-based full-length cdna clones of kunjin virus, J. virol., 75, 1, 4633-4640, (2001)
[10] Krakauer, D.; Komarova, N., Levels of selection in positive-strand virus dynamics, J. evol. biol., 16, 1, 64-73, (2003)
[11] Layden-Almer, J.E.; Ribeiro, R.M.; Wiley, T.; Perelson, A.S.; Layden, T.J., Viral dynamics and response differences in HCV-infected african American and white patients treated with IFN and ribavirin, Hepatology, 37, 6, 1343-1350, (2003)
[12] Levin, B.R.; Bull, J.J., Short-sighted evolution and the virulence of pathogenic microorganisms, Trends microbiol., 2, 3, 76-81, (1994)
[13] Lohmann, V.; Korner, F.; Koch, J.; Herian, U.; Theilmann, L.; Bartenschlager, R., Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line, Science, 285, 5424, 110-112, (1999)
[14] Lohmann, V.; Roos, A.; Korner, F.; Koch, J.; Bartenschlager, R., Biochemical and kinetic analysis of NS5B RNA-dependent RNA polymerase of the hepatitis C virus, Virology, 249, 1, 108-118, (1998)
[15] Moradpour, D.; Gosert, R.; Egger, D.; Penin, F.; Blum, H.; Bienz, K., Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex, Antiviral res., 60, 2, 103-109, (2003)
[16] Nugent, C.; Johnson, K.; Sarnow, P.; Kirkegaard, K., Functional coupling between replication and packaging of poliovirus replicon RNA, J. virol., 73, 1, 427-435, (1999)
[17] Oh, J.-W.; Ito, T.; Lai, M., A recombinant hepatitis C virus RNA-dependent RNA polymerase capable of copying the full-length viral RNA, J. virol., 73, 9, 7694-7702, (1999)
[18] Petzold, L., Automatic selection of methods for solving stiff and nonstiff systems of ordinary differential equations, SIAM J. sci. stat. comput., 4, 136-148, (1983) · Zbl 0518.65051
[19] Pogue, G.; Huntley, C.; Hall, T., Common replication strategies emerging from the study of diverse groups of positive-strand RNA viruses, Arch. virol. suppl., 9, 181-194, (1994)
[20] Quinkert, D.; Bartenschlager, R.; Lohmann, V., Quantitative analysis of the hepatitis C virus replication complex, J. virol., 79, 21, 13594-13605, (2005)
[21] Regoes, R.; Crotty, S.; Antia, R.; Tanaka, M.M., Optimal replication of poliovirus within cells, Am. nat., 165, 3, 364-373, (2005)
[22] Rong, L.; Dahari, H.; Ribeiro, R.M.; Perelson, A.S., Rapid emergence of protease inhibitor resistance in hepatitis C virus, Sci. transl. med., 2, 30, 30-32, (2010)
[23] Sanchez, M.A.; Blower, S.M., Uncertainty and sensitivity analysis of the basic reproductive rate. tuberculosis as an example, Am. J. epidemiol., 145, 12, 1127-1137, (1997)
[24] Soetaert, K.; Petzoldt, T.; Setzer, R.W., Desolve: general solvers for initial value problems of ordinary differential equations (ODE), partial differential equations (PDE) and differential algebraic equations (DAE), R package version, 1, (2009)
[25] Stearns, S.C., Evolution of life histories, (1992), Oxford University Press Oxford
[26] Thébaud, G.; Chadoeuf, J.; Morelli, M.J.; McCauley, J.W.; Haydon, D.T., The relationship between mutation frequency and replication strategy in positive-sense single-stranded RNA viruses, Proc. biol. sci., 277, 1682, 809-817, (2010)
[27] Venter, P.; Krishna, N.; Schneemann, A., Capsid protein synthesis from replicating RNA directs specific packaging of the genome of a multipartite, positive-strand RNA virus, J. virol., 79, 10, 6248-6293, (2005)
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