Single-cell analysis and stochastic modelling unveil large cell-to-cell variability in influenza A virus infection

Nature Communications

Volumn 6, Issue , 2015, Pages

  Heldt, Frank S ^a   Kupke, Sascha Y ^a   Dorl, Sebastian ^a   Reichl, Udo ^a,b   Frensing, Timo ^a,b  

^a MAX PLANCK INSTITUTE FOR DYNAMICS OF COMPLEX TECHNICAL SYSTEMS   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

CYTOLOGY; GENOME; HETEROGENEITY; INFLUENZA; MODELING; RNA; STOCHASTICITY;

ANIMAL CELL; ARTICLE; CELL HETEROGENEITY; CELL LEVEL; CONTROLLED STUDY; INFLUENZA A; NONHUMAN; PLAQUE FORMING CELL; RNA DEGRADATION; SIMULATION; SINGLE CELL ANALYSIS; STOCHASTIC MODEL; VIRUS ENTRY; VIRUS GENOME; VIRUS REPLICATION; VIRUS TITRATION; ANIMAL; CELL LINE; CELL SURVIVAL; CHEMISTRY; GENETICS; HUMAN; INFLUENZA; INFLUENZA A VIRUS; KINETICS; PATHOPHYSIOLOGY; PHYSIOLOGY; THEORETICAL MODEL; VIROLOGY;

INFLUENZA A VIRUS;

ANIMALS; CELL LINE; CELL SURVIVAL; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; KINETICS; MODELS, THEORETICAL; SINGLE-CELL ANALYSIS;

EID: 84947782751     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9938     Document Type: Article

References (37)

1. Raj, A., van Oudenaarden, A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226 (2008).
2. Delbruck, M. The burst size distribution in the growth of bacterial viruses (bacteriophages). J. Bacteriol. 50, 131-135 (1945).
3. Zhu, Y., Yongky, A., Yin, J. Growth of an RNA virus in single cells reveals a broad fitness distribution. Virology 385, 39-46 (2009).
4. Timm, A., Yin, J. Kinetics of virus production from single cells. Virology 424, 11-17 (2012).
5. Elowitz, M. B., Levine, A. J., Siggia, E. D., Swain, P. S. Stochastic gene expression in a single cell. Science 297, 1183-1186 (2002).
6. Snijder, B. et al. Population context determines cell-to-cell variability in endocytosis and virus infection. Nature 461, 520-523 (2009).
7. Hensel, S. C., Rawlings, J. B., Yin, J. Stochastic kinetic modeling of vesicular stomatitis virus intracellular growth. Bull. Math. Biol. 71, 1671-1692 (2009).
8. Schulte, M. B., Andino, R. Single-cell analysis uncovers extensive biological noise in poliovirus replication. J. Virol. 88, 6205-6212 (2014).
9. Genzel, Y., Reichl, U. Continuous cell lines as a production system for influenza vaccines. Expert Rev. Vaccines 8, 1681-1692 (2009).
10. Wood, J. M., Robertson, J. S. From lethal virus to life-saving vaccine: developing inactivated vaccines for pandemic influenza. Nat. Rev. Microbiol. 2, 842-847 (2004).
11. Shaw, M. L., Palese, P. in Fields Virology 6th edn (eds Fields, B. N., Knipe, D. M.) Vol. I, 1151-1185 (Wolters Kluwer Lippincott Williams: Philadelphia, 2013).
12. Fodor, E. The RNA polymerase of influenza a virus: mechanisms of viral transcription and replication. Acta Virol. 57, 113-122 (2013).
13. Eisfeld, A. J., Neumann, G., Kawaoka, Y. At the centre: influenza A virus ribonucleoproteins. Nat. Rev. Microbiol. 13, 28-41 (2015).
14. Heldt, F. S. et al. Multiscale modeling of influenza A virus infection supports the development of direct-acting antivirals. PLoS Comput. Biol. 9, e1003372 (2013).
15. Heldt, F. S., Frensing, T., Reichl, U. Modeling the intracellular dynamics of influenza virus replication to understand the control of viral RNA synthesis. J. Virol. 86, 7806-7817 (2012).
16. Koff, W. C., Knight, V. Inhibition of influenza virus uncoating by rimantadine hydrochloride. J. Virol. 31, 261-263 (1979).
17. Stegmann, T. et al. Evaluation of viral membrane fusion assays. Comparison of the octadecylrhodamine dequenching assay with the pyrene excimer assay. Biochemistry 32, 11330-11337 (1993).
18. Dulbecco, R., Vogt, M. One-step growth curve of Western equine encephalomyelitis virus on chicken embryo cells grown in vitro and analysis of virus yields from single cells. J. Exp. Med. 99, 183-199 (1954).
19. Delbrück, M. Statistical fluctuations in autocatalytic reactions. J. Chem. Phys. 8, 120-124 (1940).
20. Koch, A. L. The logarithm in biology. 1. Mechanisms generating the log-normal distribution exactly. J. Theor. Biol. 12, 276-290 (1966).
21. Furusawa, C., Suzuki, T., Kashiwagi, A., Yomo, T., Kaneko, K. Ubiquity of log-normal distributions in intra-cellular reaction dynamics. Biophysics (Oxf). 1, 25-31 (2005).
22. Boucrot, E., Kirchhausen, T. Mammalian cells change volume during mitosis. PLoS ONE 3, e1477 (2008).
23. Brunotte, L. et al. The nuclear export protein of H5N1 influenza A viruses recruits Matrix 1 (M1) protein to the viral ribonucleoprotein to mediate nuclear export. J. Biol. Chem. 289, 20067-20077 (2014).
24. Brooke, C. B. et al. Most influenza a virions fail to express at least one essential viral protein. J. Virol. 87, 3155-3162 (2013).
25. Srivastava, R., You, L., Summers, J., Yin, J. Stochastic vs. deterministic modeling of intracellular viral kinetics. J. Theor. Biol. 218, 309-321;2002
26. Stiefel, P. et al. Cooperative vaccinia infection demonstrated at the single-cell level using FluidFM. Nano Lett. 12, 4219-4227 (2012).
27. Svec, D. et al. Direct cell lysis for single-cell gene expression profiling. Front. Oncol. 3, 274 (2013).
28. Kawakami, E. et al. Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA. J. Virol. Methods 173, 1-6 (2011).
29. Nunes-Correia, I., Ramalho-Santos, J., Nir, S., Pedroso de Lima, M. C. Interactions of influenza virus with cultured cells: detailed kinetic modeling of binding and endocytosis. Biochemistry 38, 1095-1101 (1999).
30. Chou, Y. Y. et al. Colocalization of different influenza viral RNA segments in the cytoplasm before viral budding as shown by single-molecule sensitivity FISH analysis. PLoS Pathog. 9, e1003358 (2013).
31. Vreede, F. T., Jung, T. E., Brownlee, G. G. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J. Virol. 78, 9568-9572 (2004).
32. Hatada, E., Hasegawa, M., Mukaigawa, J., Shimizu, K., Fukuda, R. Control of influenza virus gene expression: quantitative analysis of each viral RNA species in infected cells. J. Biochem. 105, 537-546 (1989).
33. Enami, M., Fukuda, R., Ishihama, A. Transcription and replication of eight RNA segments of influenza virus. Virology 142, 68-77 (1985).
34. Portela, A., Digard, P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 83, 723-734 (2002).
35. Gillespie, D. T. Stochastic simulation of chemical kinetics. Annu. Rev. Phys. Chem. 58, 35-55 (2007).
36. McCollum, J. M., Peterson, G. D., Cox, C. D., Simpson, M. L., Samatova, N. F. The sorting direct method for stochastic simulation of biochemical systems with varying reaction execution behavior. Comput. Biol. Chem. 30, 39-49 (2006).
37. Cao, Y., Gillespie, D. T., Petzold, L. R. Efficient step size selection for the tauleaping simulation method. J. Chem. Phys. 124, 044109 (2006).