A Method to Determine the Duration of the Eclipse Phase for in Vitro Infection with a Highly Pathogenic SHIV Strain

Overview

Journal Sci Rep

Specialty Science

Date 2015 May 22

PMID 25996439

Citations 26

Authors

Yusuke Kakizoe

Shinji Nakaoka

Catherine A A Beauchemin

Satoru Morita

Hiromi Mori

Tatsuhiko Igarashi

Kazuyuki Aihara

Tomoyuki Miura

Shingo Iwami

Affiliations

Soon will be listed here.

Abstract

The time elapsed between successful cell infection and the start of virus production is called the eclipse phase. Its duration is specific to each virus strain and, along with an effective virus production rate, plays a key role in infection kinetics. How the eclipse phase varies amongst cells infected with the same virus strain and therefore how best to mathematically represent its duration is not clear. Most mathematical models either neglect this phase or assume it is exponentially distributed, such that at least some if not all cells can produce virus immediately upon infection. Biologically, this is unrealistic (one must allow for the translation, transcription, export, etc. to take place), but could be appropriate if the duration of the eclipse phase is negligible on the time-scale of the infection. If it is not, however, ignoring this delay affects the accuracy of the mathematical model, its parameter estimates, and predictions. Here, we introduce a new approach, consisting in a carefully designed experiment and simple analytical expressions, to determine the duration and distribution of the eclipse phase in vitro. We find that the eclipse phase of SHIV-KS661 lasts on average one day and is consistent with an Erlang distribution.

Citing Articles

Incorporating Intracellular Processes in Virus Dynamics Models.

Ciupe S, Conway J Microorganisms. 2024; 12(5).

PMID: 38792730 PMC: 11124127. DOI: 10.3390/microorganisms12050900.

The effect of random virus failure following cell entry on infection outcome and the success of antiviral therapy.

Quirouette C, Cresta D, Li J, Wilkie K, Liang H, Beauchemin C Sci Rep. 2023; 13(1):17243.

PMID: 37821517 PMC: 10567758. DOI: 10.1038/s41598-023-44180-w.

Multiple cohort study of hospitalized SARS-CoV-2 in-host infection dynamics: Parameter estimates, identifiability, sensitivity and the eclipse phase profile.

Korosec C, Betti M, Dick D, Ooi H, Moyles I, Wahl L J Theor Biol. 2023; 564:111449.

PMID: 36894132 PMC: 9990894. DOI: 10.1016/j.jtbi.2023.111449.

Initial Inoculum and the Severity of COVID-19: A Mathematical Modeling Study of the Dose-Response of SARS-CoV-2 Infections.

Fain B, Dobrovolny H Epidemiologia (Basel). 2022; 1(1):5-15.

PMID: 36417207 PMC: 9620883. DOI: 10.3390/epidemiologia1010003.

Fractional transit compartment model for describing drug delayed response to tumors using Mittag-Leffler distribution on age-structured PKPD model.

Byun J, Roh Y, Yoon I, Kim K, Jung I PLoS One. 2022; 17(11):e0276654.

PMID: 36331932 PMC: 9635704. DOI: 10.1371/journal.pone.0276654.

References

Rong L, Guedj J, Dahari H, Coffield Jr D, Levi M, Smith P . Analysis of hepatitis C virus decline during treatment with the protease inhibitor danoprevir using a multiscale model. PLoS Comput Biol. 2013; 9(3):e1002959. PMC: 3597560. DOI: 10.1371/journal.pcbi.1002959. View

GAUSH C, Smith T . Replication and plaque assay of influenza virus in an established line of canine kidney cells. Appl Microbiol. 1968; 16(4):588-94. PMC: 547475. DOI: 10.1128/am.16.4.588-594.1968. View

Perelson A . Modelling viral and immune system dynamics. Nat Rev Immunol. 2002; 2(1):28-36. DOI: 10.1038/nri700. View

Little S, McLean A, Spina C, Richman D, Havlir D . Viral dynamics of acute HIV-1 infection. J Exp Med. 1999; 190(6):841-50. PMC: 2195636. DOI: 10.1084/jem.190.6.841. View

Petravic J, Ellenberg P, Chan M, Paukovics G, Smyth R, Mak J . Intracellular dynamics of HIV infection. J Virol. 2013; 88(2):1113-24. PMC: 3911679. DOI: 10.1128/JVI.02038-13. View

Freed E . HIV-1 replication. Somat Cell Mol Genet. 2002; 26(1-6):13-33. DOI: 10.1023/a:1021070512287. View

Clapham P, Weiss R, Dalgleish A, EXLEY M, Whitby D, Hogg N . Human immunodeficiency virus infection of monocytic and T-lymphocytic cells: receptor modulation and differentiation induced by phorbol ester. Virology. 1987; 158(1):44-51. DOI: 10.1016/0042-6822(87)90236-4. View

Shinohara K, Sakai K, Ando S, Ami Y, Yoshino N, Takahashi E . A highly pathogenic simian/human immunodeficiency virus with genetic changes in cynomolgus monkey. J Gen Virol. 1999; 80 ( Pt 5):1231-1240. DOI: 10.1099/0022-1317-80-5-1231. View

Jordan A, Defechereux P, Verdin E . The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. EMBO J. 2001; 20(7):1726-38. PMC: 145503. DOI: 10.1093/emboj/20.7.1726. View

10.

Ribeiro R, Qin L, Chavez L, Li D, Self S, Perelson A . Estimation of the initial viral growth rate and basic reproductive number during acute HIV-1 infection. J Virol. 2010; 84(12):6096-102. PMC: 2876646. DOI: 10.1128/JVI.00127-10. View

11.

Holder B, Beauchemin C . Exploring the effect of biological delays in kinetic models of influenza within a host or cell culture. BMC Public Health. 2011; 11 Suppl 1:S10. PMC: 3317580. DOI: 10.1186/1471-2458-11-S1-S10. View

12.

Nelson P, Perelson A . Mathematical analysis of delay differential equation models of HIV-1 infection. Math Biosci. 2002; 179(1):73-94. DOI: 10.1016/s0025-5564(02)00099-8. View

13.

Pinilla L, Holder B, Abed Y, Boivin G, Beauchemin C . The H275Y neuraminidase mutation of the pandemic A/H1N1 influenza virus lengthens the eclipse phase and reduces viral output of infected cells, potentially compromising fitness in ferrets. J Virol. 2012; 86(19):10651-60. PMC: 3457267. DOI: 10.1128/JVI.07244-11. View

14.

Kim S, Byrn R, Groopman J, Baltimore D . Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: evidence for differential gene expression. J Virol. 1989; 63(9):3708-13. PMC: 250962. DOI: 10.1128/JVI.63.9.3708-3713.1989. View

15.

Guedj J, Rong L, Dahari H, Perelson A . A perspective on modelling hepatitis C virus infection. J Viral Hepat. 2010; 17(12):825-33. PMC: 3070361. DOI: 10.1111/j.1365-2893.2010.01348.x. View

16.

Nelson P, Murray J, Perelson A . A model of HIV-1 pathogenesis that includes an intracellular delay. Math Biosci. 2000; 163(2):201-15. DOI: 10.1016/s0025-5564(99)00055-3. View

17.

Polis M, Feinberg M, Grossman Z, Levi I, Jankelevich S, Yarchoan R . Ongoing HIV dissemination during HAART. Nat Med. 1999; 5(10):1099-104. DOI: 10.1038/13410. View

18.

Weinberger L, Burnett J, Toettcher J, Arkin A, Schaffer D . Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell. 2005; 122(2):169-82. DOI: 10.1016/j.cell.2005.06.006. View

19.

Kozyrev I, Ibuki K, Shimada T, Kuwata T, Takemura T, Hayami M . Characterization of less pathogenic infectious molecular clones derived from acute-pathogenic SHIV-89.6p stock virus. Virology. 2001; 282(1):6-13. DOI: 10.1006/viro.2000.0839. View

20.

Iwami S, Holder B, Beauchemin C, Morita S, Tada T, Sato K . Quantification system for the viral dynamics of a highly pathogenic simian/human immunodeficiency virus based on an in vitro experiment and a mathematical model. Retrovirology. 2012; 9:18. PMC: 3305505. DOI: 10.1186/1742-4690-9-18. View