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Should a viral genome stay in the host cell or leave? A quantitative dynamics study of how hepatitis C virus deals with this dilemma

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  • Shoya Iwanami
  • Kosaku Kitagawa
  • Hirofumi Ohashi
  • Yusuke Asai
  • Kaho Shionoya
  • Wakana Saso
  • Kazane Nishioka
  • Hisashi Inaba
  • Shinji Nakaoka
  • Takaji Wakita
  • Odo Diekmann
  • Shingo Iwami
  • Koichi Watashi

Abstract

Virus proliferation involves gene replication inside infected cells and transmission to new target cells. Once positive-strand RNA virus has infected a cell, the viral genome serves as a template for copying (“stay-strategy”) or is packaged into a progeny virion that will be released extracellularly (“leave-strategy”). The balance between genome replication and virion release determines virus production and transmission efficacy. The ensuing trade-off has not yet been well characterized. In this study, we use hepatitis C virus (HCV) as a model system to study the balance of the two strategies. Combining viral infection cell culture assays with mathematical modeling, we characterize the dynamics of two different HCV strains (JFH-1, a clinical isolate, and Jc1-n, a laboratory strain), which have different viral release characteristics. We found that 0.63% and 1.70% of JFH-1 and Jc1-n intracellular viral RNAs, respectively, are used for producing and releasing progeny virions. Analysis of the Malthusian parameter of the HCV genome (i.e., initial proliferation rate) and the number of de novo infections (i.e., initial transmissibility) suggests that the leave-strategy provides a higher level of initial transmission for Jc1-n, whereas, in contrast, the stay-strategy provides a higher initial proliferation rate for JFH-1. Thus, theoretical-experimental analysis of viral dynamics enables us to better understand the proliferation strategies of viruses, which contributes to the efficient control of virus transmission. Ours is the first study to analyze the stay-leave trade-off during the viral life cycle and the significance of the replication-release switching mechanism for viral proliferation.A theoretical-experimental analysis of viral dynamics reveals a stay/leave trade-off during the viral life cycle and demonstrates the significance for viral proliferation of a replication-release switching mechanism.

Suggested Citation

  • Shoya Iwanami & Kosaku Kitagawa & Hirofumi Ohashi & Yusuke Asai & Kaho Shionoya & Wakana Saso & Kazane Nishioka & Hisashi Inaba & Shinji Nakaoka & Takaji Wakita & Odo Diekmann & Shingo Iwami & Koichi , 2020. "Should a viral genome stay in the host cell or leave? A quantitative dynamics study of how hepatitis C virus deals with this dilemma," PLOS Biology, Public Library of Science, vol. 18(7), pages 1-17, July.
    • Handle: RePEc:plo:pbio00:3000562
    DOI: 10.1371/journal.pbio.3000562
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    References listed on IDEAS

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    1. Libin Rong & Jeremie Guedj & Harel Dahari & Daniel J Coffield Jr & Micha Levi & Patrick Smith & Alan S Perelson, 2013. "Analysis of Hepatitis C Virus Decline during Treatment with the Protease Inhibitor Danoprevir Using a Multiscale Model," PLOS Computational Biology, Public Library of Science, vol. 9(3), pages 1-12, March.
    2. Soetaert, Karline & Petzoldt, Thomas, 2010. "Inverse Modelling, Sensitivity and Monte Carlo Analysis in R Using Package FME," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 33(i03).
    3. Tim Maiwald & Helge Hass & Bernhard Steiert & Joep Vanlier & Raphael Engesser & Andreas Raue & Friederike Kipkeew & Hans H Bock & Daniel Kaschek & Clemens Kreutz & Jens Timmer, 2016. "Driving the Model to Its Limit: Profile Likelihood Based Model Reduction," PLOS ONE, Public Library of Science, vol. 11(9), pages 1-18, September.
    4. Пигнастый, Олег & Koжевников, Георгий, 2019. "Распределенная Динамическая Pde-Модель Программного Управления Загрузкой Технологического Оборудования Производственной Линии [Distributed dynamic PDE-model of a program control by utilization of t," MPRA Paper 93278, University Library of Munich, Germany, revised 02 Feb 2019.
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