High-throughput single-cell kinetics of virus infections in the presence of defective interfering particles

Journal of Virology

Volumn 90, Issue 3, 2016, Pages 1599-1612

  Akpinar, Fulya ^a,b   Timm, Andrea ^a,c   Yin, John ^a  

^a University of Wisconsin Madison   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BHK CELL LINE; CELL DENSITY; CELL INTERACTION; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; DEFECTIVE INTERFERING PARTICLE; GENE EXPRESSION; GENETIC CODE; NONHUMAN; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; VESICULOVIRUS; VIROGENESIS; VIRUS GENE; VIRUS INFECTION; VIRUS PARTICLE; VIRUS RELEASE; ANIMAL; CELL LINE; GENETICS; HAMSTER; HELPER VIRUS; METABOLISM; PHYSIOLOGY; REPORTER GENE; SATELLITE VIRUS; TIME FACTOR; VIRUS LOAD; VIRUS REPLICATION;

PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ANIMALS; CELL LINE; CRICETINAE; DEFECTIVE VIRUSES; GENES, REPORTER; HELPER VIRUSES; LUMINESCENT PROTEINS; TIME FACTORS; VESICULOVIRUS; VIRAL LOAD; VIRUS REPLICATION;

EID: 84958078465     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02190-15     Document Type: Article

References (73)

1. Von Magnus P. 1954. Incomplete forms of influenza virus. Adv Virus Res 2:59-79. http://dx.doi.org/10.1016/S0065-3527(08)60529-1.
2. Marcus PI, Ngunjiri JM, Sekellick MJ. 2009. Dynamics of biologically active subpopulations of influenza virus: plaque-forming, noninfectious cell-killing, and defective interfering particles. J Virol 83:8122-8130. http://dx.doi.org/10.1128/JVI.02680-08.
3. Carpenter JE, Henderson EP, Grose C. 2009. Enumeration of an extremely high particle-to-PFU ratio for varicella-zoster virus. J Virol 83: 6917-6921. http://dx.doi.org/10.1128/JVI.00081-09.
4. Huang AS, Baltimore D. 1970. Defective viral particles and viral disease processes. Nature 226:325-327. http://dx.doi.org/10.1038/226325a0.
5. Cooper PD, Bellett AJD. 1959. A transmissible interfering component of vesicular stomatitis virus preparations. J Gen Microbiol 21:485-497. http://dx.doi.org/10.1099/00221287-21-3-485.
6. Stampfer M, Baltimore D, Huang AS. 1969. Ribonucleic acid synthesis of vesicular stomatitis virus. I. Species of ribonucleic acid found in Chinese hamster ovary cells infected with plaque-forming and defective particles. J Virol 4:154-161.
7. Huang AS, Manders EK. 1972. Ribonucleic acid synthesis of vesicular stomatitis virus. IV. Transcription by standard virus in the presence of defective interfering particles. J Virol 9:909-916.
8. Lazzarini RA, Keene JD, Schubert M. 1981. The origins of defective interfering particles of the negative-strand RNA viruses. Cell 26:145-154. http://dx.doi.org/10.1016/0092-8674(81)90298-1.
9. Saira K, Lin X, DePasse JV, Halpin R, Twaddle A, Stockwell T, Angus B, Cozzi-Lepri A, Delfino M, Dugan V, Dwyer DE, Freiberg M, Horban A, Losso M, Lynfield R, Wentworth DN, Holmes EC, Davey R, Wentworth DE, Ghedin E. 2013. Sequence analysis of in vivo defective interfering-like RNA of influenza A H1N1 pandemic virus. J Virol 87:8064-8074. http://dx.doi.org/10.1128/JVI.00240-13.
10. Aaskov J, Buzacott K, Thu HM, Lowry K, Holmes EC. 2006. Long-term transmission of defective RNA viruses in humans and Aedes mosquitoes. Science 311:236-238. http://dx.doi.org/10.1126/science.1115030.
11. Li D, Lott WB, Lowry K, Jones A, Thu HM, Aaskov J. 2011. Defective interfering viral particles in acute dengue infections. PLoS One 6:e19447. http://dx.doi.org/10.1371/journal.pone.0019447.
12. Pesko KN, Fitzpatrick KA, Ryan EM, Shi P-Y, Zhang B, Lennon NJ, Newman RM, Henn MR, Ebel GD. 2012. Internally deleted WNV genomes isolated from exotic birds in New Mexico: function in cells, mosquitoes, and mice. Virology 427:10-17. http://dx.doi.org/10.1016/j.virol.2012.01.028.
13. Sugiyama K, Suzuki K, Nakazawa T, Funami K, Hishiki T, Ogawa K, Saito S, Shimotohno KW, Suzuki T, Shimizu Y, Tobita R, Hijikata M, Takaku H, Shimotohno K. 2009. Genetic analysis of hepatitis C virus with defective genome and its infectivity in vitro. J Virol 83:6922-6928. http://dx.doi.org/10.1128/JVI.02674-08.
14. Myhre MR, Olsen G-H, Gosert R, Hirsch HH, Rinaldo CH. 2010. Clinical polyomavirus BK variants with agnogene deletion are nonfunctional but rescued by trans-complementation. Virology 398:12-20. http://dx.doi.org/10.1016/j.virol.2009.11.029.
15. Zhang D, Dong P, Zhang K, Deng L, Bach C, Chen W, Li F, Protzer U, Ding H, Zeng C. 2012. Whole genome HBV deletion profiles and the accumulation of preS deletion mutant during antiviral treatment. BMC Microbiol 12:307. http://dx.doi.org/10.1186/1471-2180-12-307.
16. Kukimoto I, Maehama T, Sekizuka T, Ogasawara Y, Kondo K, Kusumoto-Matsuo R, Mori S, Ishii Y, Takeuchi T, Yamaji T, Takeuchi F, Hanada K, Kuroda M. 2013. Genetic variation of human papillomavirus type 16 in individual clinical specimens revealed by deep sequencing. PLoS One 8:e80583. http://dx.doi.org/10.1371/journal.pone.0080583.
17. Chateigner A, Bézier A, Labrousse C, Jiolle D, Barbe V, Herniou EA. 2015. Ultra deep sequencing of a baculovirus population reveals widespread genomic variations. Viruses 7:3625-3646. http://dx.doi.org/10.3390/v7072788.
18. Calain P, Monroe MC, Nichol ST. 1999. Ebola virus defective interfering particles and persistent infection. Virology 262:114-128. http://dx.doi.org/10.1006/viro.1999.9915.
19. Kennedy JC, Macdonald RD. 1982. Persistent infection with infectious pancreatic necrosis virus mediated by defective-interfering (DI) virus particles in a cell line showing strong interference but little DI replication. J Gen Virol 58:361-371. http://dx.doi.org/10.1099/0022-1317-58-2-361.
20. Yount JS, Kraus TA, Horvath CM, Moran TM, Lopez CB. 2006. A novel role for viral-defective interfering particles in enhancing dendritic cell maturation. J Immunol 177:4503-4513. http://dx.doi.org/10.4049/jimmunol.177.7.4503.
21. Baum A, Sachidanandam R, García-Sastre A. 2010. Preference of RIG-I for short viralRNAmolecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci U S A 107:16303-16308. http://dx.doi.org/10.1073/pnas.1005077107.
22. Scott PD, Meng B, Marriott AC, Easton AJ, Dimmock NJ. 2011. Defective interfering virus protects elderly mice from influenza. Virol J 8:212. http://dx.doi.org/10.1186/1743-422X-8-212.
23. Bean WJ, Kawaoka Y, Wood JM, Pearson JE, Webster RG. 1985. Characterization of virulent and avirulent A/chicken/Pennsylvania/83 influenza A viruses: potential role of defective interfering RNAs in nature. J Virol 54:151-160.
24. Doyle M, Holland JJ. 1973. Prophylaxis and immunization in mice by use of virus-free defective T particles to protect against intracerebral infection by vesicular stomatitis virus. Proc Natl Acad Sci U S A 70:2105-2108. http://dx.doi.org/10.1073/pnas.70.7.2105.
25. Killip MJ, Young DF, Precious BL, Goodbourn S, Randall RE. 2012. Activation of the beta interferon promoter by paramyxoviruses in the absence of virus protein synthesis. J Gen Virol 93:299-307. http://dx.doi.org/10.1099/vir.0.037531-0.
26. Dimmock NJ, Easton AJ. 2014. Defective interfering influenza virus RNAs: time to reevaluate their clinical potential as broad-spectrum antivirals? J Virol 88:5217-5227. http://dx.doi.org/10.1128/JVI.03193-13.
27. Notton T, Sardanyés J, Weinberger AD, Weinberger LS. 2014. The case for transmissible antivirals to control population-wide infectious disease. Trends Biotechnol 32:400-405. http://dx.doi.org/10.1016/j.tibtech.2014.06.006.
28. Šantak M, Markušić M, Balija ML, Kopač SK, Jug R, Örvell C, Tomac J, Forčić D. 2015. Accumulation of defective interfering viral particles in only a few passages in Vero cells attenuates mumps virus neurovirulence. Microbes Infect 17:228-236. http://dx.doi.org/10.1016/j.micinf.2014.11.006.
29. Thompson KAS, Yin J. 2010. Population dynamics of an RNA virus and its defective interfering particles in passage cultures. Virol J 7:257. http://dx.doi.org/10.1186/1743-422X-7-257.
30. Timm C, Akpinar F, Yin J. 2014. Quantitative characterization of defective virus emergence by deep sequencing. J Virol 88:2623-2632. http://dx.doi.org/10.1128/JVI.02675-13.
31. Frensing T, Pflugmacher A, Bachmann M, Peschel B, Reichl U. 2014. Impact of defective interfering particles on virus replication and antiviral host response in cell culture-based influenza vaccine production. Appl Microbiol Biotechnol 98:8999-9008. http://dx.doi.org/10.1007/s00253-014-5933-y.
32. Bellett AJD, Cooper PD. 1959. Some properties of the transmissible interfering component of vesicular stomatitis virus preparations. J Gen Microbiol 21:498-509. http://dx.doi.org/10.1099/00221287-21-3-498.
33. Marcus PI, Sekellick MJ. 1974. Cell killing by viruses. I. Comparison of cell-killing, plaque-forming, and defective-interfering particles of vesicular stomatitis virus. Virology 57:321-338.
34. Khan S, Lazzarini R. 1977. The relationship between autointerference and the replication of a defective interfering particle. Virology 77:189-201. http://dx.doi.org/10.1016/0042-6822(77)90417-2.
35. DePolo NJ, Giachetti C, Holland JJ. 1987. Continuing coevolution of virus and defective interfering particles and of viral genome sequences during undiluted passages: virus mutants exhibiting nearly complete resistance to formerly dominant defective interfering particles. J Virol 61: 454-464.
36. Palma EL, Huang A. 1974. Cyclic production of vesicular stomatitis virus caused by defective interfering particles. J Infect Dis 129:402-410. http://dx.doi.org/10.1093/infdis/129.4.402.
37. Von Laer DM, Mack D, Kruppa J. 1988. Delayed formation of defective interfering particles in vesicular stomatitis virus-infected cells: kinetic studies of viral protein and RNA synthesis during autointerference. J Virol 62:1323-1329.
38. Holland JJ, Villarreal LP, Breindl M. 1976. Factors involved in the generation and replication of rhabdovirus defective T particles. J Virol 17:805-815.
39. Huang AS. 1973. Defective interfering viruses. Annu Rev Microbiol 27: 101-117. http://dx.doi.org/10.1146/annurev.mi.27.100173.000533.
40. Lim K-I, Lang T, Lam V, Yin J. 2006. Model-based design of growthattenuated viruses. PLoS Comput Biol 2:e116. http://dx.doi.org/10.1371/journal.pcbi.0020116.
41. Hensel SC, Rawlings JB, Yin J. 2009. Stochastic kinetic modeling of vesicular stomatitis virus intracellular growth. Bull Math Biol 71:1671-1692. http://dx.doi.org/10.1007/s11538-009-9419-5.
42. Timm C, Gupta A, Yin J. 2015. Robust kinetics of an RNA virus: transcription rates are set by genome levels. Biotechnol Bioeng 112:1655-1662. http://dx.doi.org/10.1002/bit.25578.
43. Blumberg BM, Kolakofsky D. 1983. An analytical review of defective infections of vesicular stomatitis virus. J Gen Virol 64:1839-1847. http://dx.doi.org/10.1099/0022-1317-64-9-1839.
44. Stauffer Thompson K, Rempala G, Yin J. 2009. Multiple-hit inhibition of infection by defective interfering particles. J Gen Virol 90:888-899. http://dx.doi.org/10.1099/vir.0.005249-0.
45. Stamminger GM, Lazzarini RA. 1977. RNA synthesis in standard and autointerfered vesicular stomatitis virus infections. Virology 77:202-211. http://dx.doi.org/10.1016/0042-6822(77)90418-4.
46. McLain L, Armstrong SJ, Dimmock NJ. 1988. One defective interfering particle per cell prevents influenza virus-mediated cytopathology: an efficient assay system. J Gen Virol 69:1415-1419. http://dx.doi.org/10.1099/0022-1317-69-6-1415.
47. Timm A, Yin J. 2012. Kinetics of virus production from single cells. Virology 424:11-17. http://dx.doi.org/10.1016/j.virol.2011.12.005.
48. Hu J, Nudelman G, Shimoni Y, Kumar M, Ding Y, López C, Hayot F, Wetmur JG, Sealfon SC. 2011. Role of cell-to-cell variability in activating a positive feedback antiviral response in human dendritic cells. PLoS One 6:e16614. http://dx.doi.org/10.1371/journal.pone.0016614.
49. Sekellick MJ, Marcus PI. 1980. Viral interference by defective particles of vesicular stomatitis virus measured in individual cells. Virology 104:247-252. http://dx.doi.org/10.1016/0042-6822(80)90385-2.
50. Schulte MB, Andino R. 2014. Single-cell analysis uncovers extensive biological noise in poliovirus replication. J Virol 88:6205-6212. http://dx.doi.org/10.1128/JVI.03539-13.
51. Zhu Y, Yongky A, Yin J. 2009. Growth of an RNA virus in single cells reveals a broad fitness distribution. Virology 385:39-46. http://dx.doi.org/10.1016/j.virol.2008.10.031.
52. Rand U, Hillebrand U, Sievers S, Willenberg S, Köster M, Hauser H, Wirth D. 2014. Uncoupling of the dynamics of host-pathogen interaction uncovers new mechanisms of viral interferon antagonism at the single-cell level. Nucleic Acids Res 42:e109. http://dx.doi.org/10.1093/nar/gku492.
53. Downey MJ, Jeziorska DM, Ott S, Tamai TK, Koentges G, Vance KW, Bretschneider T. 2011. Extracting fluorescent reporter time courses of cell lineages from high-throughput microscopy at low temporal resolution. PLoS One 6:e27886. http://dx.doi.org/10.1371/journal.pone.0027886.
54. Sáez-Cirión A, Nicola M-A, Pancino G, Shorte SL. 2006. Quantitative real-time analysis of HIV-1 gene expression dynamics in single living primary cells. Biotechnol J 1:682-689. http://dx.doi.org/10.1002/biot.200600045.
55. Knapp B, Rebhan I, Kumar A, Matula P, Kiani NA, Binder M, Erfle H, Rohr K, Eils R, Bartenschlager R, Kaderali L. 2011. Normalizing for individual cell population context in the analysis of high-content cellular screens. BMC Bioinformatics 12:485. http://dx.doi.org/10.1186/1471-2105-12-485.
56. Swick A, Baltes A, Yin J. 2014. Visualizing infection spread: dual-color fluorescent reporting of virus-host interactions. Biotechnol Bioeng 111: 1200-1209. http://dx.doi.org/10.1002/bit.25170.
57. Wertz GW, Perepelitsa VP, Ball LA. 1998. Gene rearrangement attenuates expression and lethality of a nonsegmented negative strand RNA virus. Proc Natl Acad Sci U S A 95:3501-3506. http://dx.doi.org/10.1073/pnas.95.7.3501.
58. Timm A. 2013. Development of single-cell techniques to investigate heterogeneity in virus-cell interactions. Ph. D. dissertation. University of Wisconsin-Madison, Madison, WI.
59. Waters JC. 2009. Accuracy and precision in quantitative fluorescence microscopy. J Cell Biol 185:1135-1148. http://dx.doi.org/10.1083/jcb.200903097.
60. Hudson DJ. 1971. Interval estimation from the likelihood function. J R Stat Soc Ser B 33(2):256-262.
61. Mittler JE, Sulzer B, Neumann AU, Perelson AS. 1998. Influence of delayed viral production on viral dynamics in HIV-1 infected patients. Math Biosci 152:143-163. http://dx.doi.org/10.1016/S0025-5564(98)10027-5.
62. Taniguchi Y, Choi PJ, Li G-W, Chen H, Babu M, Hearn J, Emili A, Xie XS. 2010. Quantifying E. coli proteome and transcriptome with singlemolecule sensitivity in single cells. Science 329:533-538. http://dx.doi.org/10.1126/science.1188308.
63. Sekellick MJ, Marcus PI. 1978. Persistent infection I. Interferon-inducing defective-interfering particles as mediators of cell sparing: Possible role in persistent infection by vesicular stomatitis virus. Virology 85:175-186.
64. Baum A, García-Sastre A. 2011. Differential recognition of viral RNA by RIG-I. Virulence 2:166-169. http://dx.doi.org/10.4161/viru.2.2.15481.
65. Otsuki K, Maeda J, Yamamoto H, Tsubokura M. 1979. Studies on avian infectious bronchitis virus (IBV). Arch Virol 60:249-255. http://dx.doi.org/10.1007/BF01317496.
66. Lam V, Duca KA, Yin J. 2005. Arrested spread of vesicular stomatitis virus infections in vitro depends on interferon-mediated antiviral activity. Biotechnol Bioeng 90:793-804. http://dx.doi.org/10.1002/bit.20467.
67. Azarin SM, Larson EA, Almodóvar-Cruz JM, de Pablo JJ, Palecek SP. 2012. Effects of 3D microwell culture on growth kinetics and metabolism of human embryonic stem cells. Biotechnol Appl Biochem 59:88-96. http://dx.doi.org/10.1002/bab.1003.
68. 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. http://dx.doi.org/10.1038/nature08282.
69. You L, Suthers PF, Yin J. 2002. Effects of Escherichia coli physiology on growth of phage T7 in vivo and in silico. J Bacteriol 184:1888-1894. http://dx.doi.org/10.1128/JB.184.7.1888-1894.2002.
70. Wagner RR, Snyder RM, Yamazaki S. 1970. Proteins of vesicular stomatitis virus: kinetics and cellular sites of synthesis. J Virol 5:548-558.
71. Bevis BJ, Glick BS. 2002. Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nat Biotechnol 20:83-87. http://dx.doi.org/10.1038/nbt0102-83.
72. Wagner RR, Levy AH, Snyder RM, RatcliffGA, Hyatt DF. 1963. Biologic properties of two plaque variants of vesicular stomatitis virus (Indiana serotype). J Immunol 91:112-122.
73. Giachetti C, Holland JJ. 1989. Vesicular stomatitis virus and its defective interfering particles exhibit in vitro transcriptional and replicative competition for purified L-NS polymerase molecules. Virology 170:264-267. http://dx.doi.org/10.1016/0042-6822(89)90375-9.