Single-Cell Virology: On-Chip Investigation of Viral Infection Dynamics

Cell Reports

Volumn 21, Issue 6, 2017, Pages 1692-1704

  Guo, Feng ^a   Li, Sixing ^b   Caglar, Mehmet Umut ^c   Mao, Zhangming ^a   Liu, Wu ^d   Woodman, Andrew ^d   Arnold, Jamie J ^d   Wilke, Claus O ^c   Huang, Tony Jun ^a,b   Cameron, Craig E ^b,d  

^a The Pennsylvania State University   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

live cell imaging; microfluidics; single cell analysis; stochastic gene expression; temporal dynamics; viral infection; virus host interaction

Indexed keywords

ANTIVIRUS AGENT; 2'-C-METHYLADENOSINE; ADENOSINE; GUANIDINE;

ARTICLE; CELL CYCLE PHASE; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; CYTOLYSIS; GENOTYPE; HELA S3 CELL LINE; HUMAN; HUMAN CELL; LIVE CELL IMAGING; MICROBIAL KINETICS; MICROBIAL POPULATION DYNAMICS; MICROFLUIDICS; PHENOTYPE; POLIOMYELITIS; PREDICTION; PRIORITY JOURNAL; VIROGENESIS; VIROLOGY; VIRULENCE; VIRUS CHARACTERIZATION; VIRUS REPLICATION; ANALOGS AND DERIVATIVES; DRUG EFFECT; FLUORESCENCE MICROSCOPY; HELA CELL LINE; HOST PATHOGEN INTERACTION; LAB ON A CHIP; PHYSIOLOGY; POLIOMYELITIS VIRUS; SINGLE CELL ANALYSIS; TIME LAPSE IMAGING;

ADENOSINE; ANTIVIRAL AGENTS; GUANIDINE; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LAB-ON-A-CHIP DEVICES; MICROSCOPY, FLUORESCENCE; POLIOVIRUS; SINGLE-CELL ANALYSIS; TIME-LAPSE IMAGING; VIRUS REPLICATION;

EID: 85034112659     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.10.051     Document Type: Article

References (35)

1. Aguilera, E.R., Erickson, A.K., Jesudhasan, P.R., Robinson, C.M., Pfeiffer, J.K., Plaques formed by mutagenized viral populations have elevated coinfection frequencies. MBio, 2017, 10.1128/mBio.02020-16 Published online March 14, 2017.
2. Akpinar, F., Timm, A., Yin, J., High-throughput single-cell kinetics of virus infections in the presence of defective interfering particles. J. Virol. 90 (2015), 1599–1612.
3. Appleby, T.C., Perry, J.K., Murakami, E., Barauskas, O., Feng, J., Cho, A., Fox, D. 3rd, Wetmore, D.R., McGrath, M.E., Ray, A.S., et al. Viral replication. Structural basis for RNA replication by the hepatitis C virus polymerase. Science 347 (2015), 771–775.
4. Arias, A., Thorne, L., Ghurburrun, E., Bailey, D., Goodfellow, I., Norovirus polymerase fidelity contributes to viral transmission in vivo. MSphere, 2016, 10.1128/mSphere.00279-16 Published online October 26, 2016.
5. Arnold, J.J., Vignuzzi, M., Stone, J.K., Andino, R., Cameron, C.E., Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. J. Biol. Chem. 280 (2005), 25706–25716.
6. Battich, N., Stoeger, T., Pelkmans, L., Control of transcript variability in single mammalian cells. Cell 163 (2015), 1596–1610.
7. Caglar, M.U., Teufel, A.I., Wilke, C.O., Sicegar: R package for sigmoidal and double-sigmoidal curve fitting. PeerJ Preprints, 5, 2017, e3116v1.
8. Carroll, S.S., Tomassini, J.E., Bosserman, M., Getty, K., Stahlhut, M.W., Eldrup, A.B., Bhat, B., Hall, D., Simcoe, A.L., LaFemina, R., et al. Inhibition of hepatitis C virus RNA replication by 2′-modified nucleoside analogs. J. Biol. Chem. 278 (2003), 11979–11984.
9. Combe, M., Garijo, R., Geller, R., Cuevas, J.M., Sanjuán, R., Single-cell analysis of RNA virus infection identifies multiple genetically diverse viral genomes within single infectious units. Cell Host Microbe 18 (2015), 424–432.
10. Crotty, S., Hix, L., Sigal, L.J., Andino, R., Poliovirus pathogenesis in a new poliovirus receptor transgenic mouse model: Age-dependent paralysis and a mucosal route of infection. J. Gen. Virol. 83 (2002), 1707–1720.
11. Domingo, E., Holland, J.J., RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51 (1997), 151–178.
12. Dulbecco, R., Production of plaques in monolayer tissue cultures by single particles of an animal virus. Proc. Natl. Acad. Sci. USA 38 (1952), 747–752.
13. Dulbecco, R., Vogt, M., Plaque formation and isolation of pure lines with poliomyelitis viruses. J. Exp. Med. 99 (1954), 167–182.
14. Ellis, E.L., Delbrück, M., The growth of bacteriophage. J. Gen. Physiol. 22 (1939), 365–384.
15. Gawad, C., Koh, W., Quake, S.R., Single-cell genome sequencing: Current state of the science. Nat. Rev. Genet. 17 (2016), 175–188.
16. Heath, J.R., Ribas, A., Mischel, P.S., Single-cell analysis tools for drug discovery and development. Nat. Rev. Drug Discov. 15 (2016), 204–216.
17. Heldt, F.S., Kupke, S.Y., Dorl, S., Reichl, U., Frensing, T., Single-cell analysis and stochastic modelling unveil large cell-to-cell variability in influenza A virus infection. Nat. Commun., 6, 2015, 8938.
18. Kallman, F., Williams, R.C., Dulbecco, R., Vogt, M., Fine structure of changes produced in cultured cells sampled at specified intervals during a single growth cycle of polio virus. J. Biophys. Biochem. Cytol. 4 (1958), 301–308.
19. Kolodziejczyk, A.A., Kim, J.K., Svensson, V., Marioni, J.C., Teichmann, S.A., The technology and biology of single-cell RNA sequencing. Mol. Cell 58 (2015), 610–620.
20. Korboukh, V.K., Lee, C.A., Acevedo, A., Vignuzzi, M., Xiao, Y., Arnold, J.J., Hemperly, S., Graci, J.D., August, A., Andino, R., Cameron, C.E., RNA virus population diversity, an optimum for maximal fitness and virulence. J. Biol. Chem. 289 (2014), 29531–29544.
21. Kuss, S.K., Etheredge, C.A., Pfeiffer, J.K., Multiple host barriers restrict poliovirus trafficking in mice. PLoS Pathog., 4, 2008, e1000082.
22. Lauring, A.S., Andino, R., Quasispecies theory and the behavior of RNA viruses. PLoS Pathog., 6, 2010, e1001005.
23. Lwoff, A., Dulbecco, R., Vogt, M., Lwoff, M., Kinetics of the release of poliomyelitis virus from single cells. Virology 1 (1955), 128–139.
24. Murakami, E., Tolstykh, T., Bao, H., Niu, C., Steuer, H.M., Bao, D., Chang, W., Espiritu, C., Bansal, S., Lam, A.M., et al. Mechanism of activation of PSI-7851 and its diastereoisomer PSI-7977. J. Biol. Chem. 285 (2010), 34337–34347.
25. Pelkmans, L., Cell Biology. Using cell-to-cell variability—a new era in molecular biology. Science 336 (2012), 425–426.
26. Pfeiffer, J.K., Kirkegaard, K., Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog., 1, 2005, e11.
27. Saadatpour, A., Lai, S., Guo, G., Yuan, G.C., Single-cell analysis in cancer genomics. Trends Genet. 31 (2015), 576–586.
28. Schulte, M.B., Andino, R., Single-cell analysis uncovers extensive biological noise in poliovirus replication. J. Virol. 88 (2014), 6205–6212.
29. Snijder, B., Pelkmans, L., Origins of regulated cell-to-cell variability. Nat. Rev. Mol. Cell Biol. 12 (2011), 119–125.
30. Symmons, O., Raj, A., What's luck got to do with it: Single cells, multiple fates, and biological nondeterminism. Mol. Cell 62 (2016), 788–802.
31. Thompson, K.A., Yin, J., Population dynamics of an RNA virus and its defective interfering particles in passage cultures. Virol. J., 7, 2010, 257.
32. Van Slyke, G.A., Arnold, J.J., Lugo, A.J., Griesemer, S.B., Moustafa, I.M., Kramer, L.D., Cameron, C.E., Ciota, A.T., Sequence-specific fidelity alterations associated with west nile virus attenuation in mosquitoes. PLoS Pathog., 11, 2015, e1005009.
33. Vignuzzi, M., Stone, J.K., Arnold, J.J., Cameron, C.E., Andino, R., Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439 (2006), 344–348.
34. Warrick, J.W., Timm, A., Swick, A., Yin, J., Tools for single-cell kinetic analysis of virus-host interactions. PLoS ONE, 11, 2016, e0145081.
35. Zeng, J., Wang, H., Xie, X., Yang, D., Zhou, G., Yu, L., An increased replication fidelity mutant of foot-and-mouth disease virus retains fitness in vitro and virulence in vivo. Antiviral Res. 100 (2013), 1–7.