Single-cell analysis of the impact of host cell heterogeneity on infection with foot-andmouth disease virus

Journal of Virology

Volumn 92, Issue 9, 2018, Pages

  Xin, Xiu ^a   Wang, Hailong ^a   Han, Lingling ^a   Wang, Mingzhen ^a   Fang, Hui ^a   Hao, Yao ^a   Li, Jiadai ^a   Zhang, Hu ^a   Zheng, Congyi ^a   Shen, Chao ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Cell cycle; Cell inclusion; Cell size; Cell sorting; FMDV

Indexed keywords

INTEGRIN RECEPTOR; VIRAL PROTEIN; VIRUS RNA;

ARTICLE; CELL HETEROGENEITY; CELL INCLUSION; CELL SIZE; CONTROLLED STUDY; CORRELATIONAL STUDY; DNA CONTENT; FLUORESCENCE ACTIVATED CELL SORTING; FOOT AND MOUTH DISEASE; FOOT AND MOUTH DISEASE VIRUS; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SINGLE CELL ANALYSIS; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS REPLICATION; VIRUS TITRATION; ANIMAL; CELL LINE; GENETICS; HAMSTER; M PHASE CELL CYCLE CHECKPOINT; PHYSIOLOGY; PROCEDURES; VIROLOGY; VIRUS LOAD;

ANIMALS; CELL LINE; CELL SIZE; CRICETINAE; FOOT-AND-MOUTH DISEASE; FOOT-AND-MOUTH DISEASE VIRUS; GENOME, VIRAL; M PHASE CELL CYCLE CHECKPOINTS; RNA, VIRAL; SINGLE-CELL ANALYSIS; VIRAL LOAD; VIRUS REPLICATION;

EID: 85045523307     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00179-18     Document Type: Article

References (45)

1. Cohen AA, Geva-Zatorsky N, Eden E, Frenkel-Morgenstern M, Issaeva I, Sigal A, Milo R, Cohen-Saidon C, Liron Y, Kam Z, Cohen L, Danon T, Perzov N, Alon U. 2008. Dynamic proteomics of individual cancer cells in response to a drug. Science 322:1511-1516. https://doi.org/10.1126/ science.1160165
2. Navin N, Kendall J, Troge J, Andrews P, Rodgers L, McIndoo J, Cook K, Stepansky A, Levy D, Esposito D, Muthuswamy L, Krasnitz A, McCombie WR, Hicks J, Wigler M. 2011. Tumour evolution inferred by single-cell sequencing. Nature 472:90-U119. https://doi.org/10.1038/nature09807
3. Raj A, Rifkin SA, Andersen E, van Oudenaarden A. 2010. Variability in gene expression underlies incomplete penetrance. Nature 463: 913-U984. https://doi.org/10.1038/nature08781
4. Rosenfeld N, Young JW, Alon U, Swain PS, Elowitz MB. 2005. Gene regulation at the single-cell level. Science 307:1962-1965. https://doi .org/10.1126/science.1106914
5. Warrick JW, Timm A, Swick A, Yin J. 2016. Tools for single-cell kinetic analysis of virus-host interactions. PLoS One 11:e0145081. https://doi .org/10.1371/journal.pone.0145081
6. Konry T, Sarkar S, Sabhachandani P, Cohen N. 2016. Innovative tools and technology for analysis of single cells and cell-cell interaction. Annu Rev Biomed Eng 18:259-284. https://doi.org/10.1146/annurev-bioeng-090215-112735
7. Raj A, van Oudenaarden A. 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216-226. https://doi .org/10.1016/j.cell.2008.09.050
8. Kannan RP, Hensley LL, Evers LE, Lemon SM, McGivern DR. 2011. Hepatitis C virus infection causes cell cycle arrest at the level of initiation of mitosis. J Virol 85:7989-8001. https://doi.org/10.1128/JVI.00280-11
9. Izumi T, Io K, Matsui M, Shirakawa K, Shinohara M, Nagai Y, Kawahara M, Kobayashi M, Kondoh H, Misawa N, Koyanagi Y, Uchiyama T, Takaori-Kondo A. 2010. HIV-1 viral infectivity factor interacts with TP53 to induce G2 cell cycle arrest and positively regulate viral replication. Proc Natl Acad Sci U S A 107:20798-20803. https://doi.org/10.1073/pnas.1008076107
10. Timm A, Yin J. 2012. Kinetics of virus production from single cells. Virology 424:11-17. https://doi.org/10.1016/j.virol.2011.12.005
11. Zhu Y, Yongky A, Yin J. 2009. Growth of an RNA virus in single cells reveals a broad fitness distribution. Virology 385:39-46. https://doi.org/ 10.1016/j.virol.2008.10.031
12. Delatorre JC, Martinezsalas E, Diez J, Domingo E. 1989. Extensive cell heterogeneity during persistent infection with foot-and-mouth-disease virus. J Virology 63:59-63
13. Caridi F, Vazquez-Calvo A, Sobrino F, Martin-Acebes MA. 2015. The pH stability of foot-and-mouth disease virus particles is modulated by residues located at the pentameric interface and in the N terminus of VP1. J Virol 89:5633-5642. https://doi.org/10.1128/JVI.03358-14
14. Huang X, Li Y, Fang H, Zheng CY. 2011. Establishment of persistent infection with foot-and-mouth disease virus in BHK-21 cells. Virol J 8:169. https://doi.org/10.1186/1743-422X-8-169
15. Huang X, Li Y, Zheng CY. 2009. A novel single-cell quantitative real-time RT-PCR method for quantifying foot-and-mouth disease viral RNA. J Virol Methods 155:150-156. https://doi.org/10.1016/j.jviromet.2008.10.007
16. Combe M, Garijo R, Geller R, Cuevas JM, Sanjuan R. 2015. Single-cell analysis of RNA virus infection identifies multiple genetically diverse viral genomes within single infectious units. Cell Host Microbe 18:424-432. https://doi.org/10.1016/j.chom.2015.09.009
17. Ciuffi A, Rato S, Telenti A. 2016. Single-cell genomics for virology. Viruses 8(5):E123. https://doi.org/10.3390/v8050123
18. Rato S, Golumbeanu M, Telenti A, Ciuffi A. 2017. Exploring viral infection using single-cell sequencing. Virus Res 239:55-68. https://doi.org/10 .1016/j.virusres.2016.10.016
19. Buettner F, Natarajan KN, Casale FP, Proserpio V, Scialdone A, Theis FJ, Teichmann SA, Marioni JC, Stegle O. 2015. Computational analysis of cell-to-cell heterogeneity in single-cell RNA-sequencing data reveals hidden subpopulations of cells. Nat Biotechnol 33:155-160. https://doi .org/10.1038/nbt.3102
20. Gao Y, Sun SQ, Guo HC. 2016. Biological function of foot-and-mouth disease virus non-structural proteins and non-coding elements. Virol J 13:107. https://doi.org/10.1186/s12985-016-0561-z
21. Stenfeldt C, Eschbaumer M, Rekant SI, Pacheco JM, Smoliga GR, Hartwig EJ, Rodriguez LL, Arzt J. 2016. The foot-and-mouth disease carrier state divergence in cattle. J Virol 90:6344-6364. https://doi.org/10.1128/JVI .00388-16
22. Martin-Acebes MA, Herrera M, Armas-Portela R, Domingo E, Sobrino F. 2010. Cell density-dependent expression of viral antigens during persistence of foot-and-mouth disease virus in cell culture. Virology 403: 47-55. https://doi.org/10.1016/j.virol.2010.04.005
23. Kopliku L, Relmy A, Romey A, Gorna K, Zientara S, Bakkali-Kassimi L, Blaise-Boisseau S. 2015. Establishment of persistent foot-and-mouth disease virus (FMDV) infection in MDBK cells. Arch Virol 160:2503-2516. https://doi.org/10.1007/s00705-015-2526-8
24. de la Torre JC, Davila M, Sobrino F, Ortin J, Domingo E. 1985. Establishment of cell lines persistently infected with foot-and-mouth disease virus. Virology 145:24-35. https://doi.org/10.1016/0042-6822(85)90198-9
25. Heldt FS, Kupke SY, Dorl S, Reichl U, Frensing T. 2015. Single-cell analysis and stochastic modelling unveil large cell-to-cell variability in influenza A virus infection. Nat Commun 6:8938. https://doi.org/10.1038/ ncomms9938
26. He Y, Xu K, Keiner B, Zhou J, Czudai V, Li T, Chen Z, Liu J, Klenk HD, Shu YL, Sun B. 2010. Influenza A virus replication induces cell cycle arrest in G0/G1 phase. J Virol 84:12832-12840. https://doi.org/10.1128/JVI.01216-10
27. Feuer R, Mena I, Pagarigan R, Slifka MK, Whitton JL. 2002. Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol 76:4430-4440. https://doi.org/10.1128/JVI.76.9.4430-4440 .2002
28. Schulte MB, Andino R. 2014. Single-cell analysis uncovers extensive biological noise in poliovirus replication. J Virol 88:6205-6212. https:// doi.org/10.1128/JVI.03539-13
29. Schmoller KM, Skotheim JM. 2015. The biosynthetic basis of cell size control. Trends Cell Biol 25:793-802. https://doi.org/10.1016/j.tcb.2015 .10.006
30. Kempe H, Schwabe A, Cremazy F, Verschure PJ, Bruggeman FJ. 2015. The volumes and transcript counts of single cells reveal concentration homeostasis and capture biological noise. Mol Biol Cell 26:797-804. https://doi.org/10.1091/mbc.E14-08-1296
31. Padovan-Merhar O, Nair GP, Biaesch AG, Mayer A, Scarfone S, Foley SW, Wu AR, Churchman LS, Singh A, Raj A. 2015. Single mammalian cells compensate for differences in cellular volume and DNA copy number through independent global transcriptional mechanisms. Mol Cell 58: 339-352. https://doi.org/10.1016/j.molcel.2015.03.005
32. Tzur A, Moore JK, Jorgensen P, Shapiro HM, Kirschner MW. 2011. Optimizing optical flow cytometry for cell volume-based sorting and analysis. PLoS One 6(1):e16053. https://doi.org/10.1371/journal.pone.0016053
33. Qi J, Liu T, Pan J, Miao P, Zhang C. 2015. Rapid baculovirus titration assay based on viable cell side scatter (SSC). Anal Chim Acta 879:58-62. https://doi.org/10.1016/j.aca.2015.04.007
34. Dove B, Brooks G, Bicknell K, Wurm T, Hiscox JA. 2006. Cell cycle perturbations induced by infection with the coronavirus infectious bronchitis virus and their effect on virus replication. J Virol 80:4147-4156. https://doi.org/10.1128/JVI.80.8.4147-4156.2006
35. Grubman MJ, Baxt B. 2004. Foot-and-mouth disease. Clin Microbiol Rev 17:465-493. https://doi.org/10.1128/CMR.17.2.465-493.2004
36. Wang G, Wang Y, Shang Y, Zhang Z, Liu X. 2015. How foot-and-mouth disease virus receptor mediates foot-and-mouth disease virus infection. Virol J 12:9. https://doi.org/10.1186/s12985-015-0246-z
37. Han SC, Guo HC, Sun SQ, Jin Y, Wei YQ, Feng X, Yao XP, Cao SZ, Liu DX, Liu XT. 2016. Productive entry of foot-and-mouth disease virus via macropinocytosis independent of phosphatidylinositol 3-kinase. Sci Rep 6:19294. https://doi.org/10.1038/srep19294
38. Snijder B, Sacher R, Rämö P, Damm E-M, Liberali P, Pelkmans L. 2009. Population context determines cell-to-cell variability in endocytosis and virus infection. Nature 461:520-523. https://doi.org/10.1038/nature08282
39. Wang LW, Chen LX, Zhu LY, Rawle M, Nie SH, Zhang J, Ping Z, Cai KR, Jacob TJC. 2002. Regulatory volume decrease is actively modulated during the cell cycle. J Cell Physiol 193:110-119. https://doi.org/10.1002/ jcp.10156
40. Schneider EL, Fowlkes BJ. 1976. Measurement of DNA content and cell volume in senescent human fibroblasts utilizing flow multiparameter single cell analysis. Exp Cell Res 98:298-302. https://doi.org/10.1016/ 0014-4827(76)90441-9
41. Wood E, Nurse P. 2015. Sizing up to divide: mitotic cell-size control in fission yeast. Annu Rev Cell Dev Biol 31:11-29. https://doi.org/10.1146/ annurev-cellbio-100814-125601
42. Li Y, Huang X, Xia B, Zheng CY. 2009. Development and validation of a duplex quantitative real-time RT-PCR assay for simultaneous detection and quantitation of foot-and-mouth disease viral positive-stranded RNAs and negative-stranded RNAs. J Virol Methods 161:161-167. https:// doi.org/10.1016/j.jviromet.2009.06.008
43. Jackson T, Clark S, Berryman S, Burman A, Cambier S, Mu DZ, Nishimura S, King AMQ. 2004. Integrin alpha v beta 8 functions as a receptor for foot-and-mouth disease virus: role of the beta-chain cytodomain in integrin-mediated infection. J Virol 78:4533-4540. https://doi.org/10 .1128/JVI.78.9.4533-4540.2004
44. Yuan B, Fang H, Shen C, Zheng CY. 2015. Expression of porcine Mx1 with FMDV IRES enhances the antiviral activity against foot-and-mouth disease virus in PK-15 cells. Arch Virol 160:1989-1999. https://doi.org/10 .1007/s00705-015-2473-4
45. Maingret N, Girardeau G, Todorova R, Goutierre M, Zugaro M. 2016. Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat Neurosci 19:959-964. https://doi.org/10.1038/nn.4304