Influenza Virus Reassortment Is Enhanced by Semi-infectious Particles but Can Be Suppressed by Defective Interfering Particles
Since the genome of an influenza A virus has eight non-contiguous segments, two influenza A viruses can exchange genes readily when they infect the same cell. This process of reassortment is important to the evolution of the virus and is one reason why this pathogen is constantly changing. It has long been known that a large proportion of the virus particles that influenza and many other RNA viruses produce are not fully infectious, but the biological significance of these particles has remained unclear. Here we show that virus particles that deliver incomplete genomes to the cell enhance the rate of reassortment. Thus, despite their limited potential to produce progeny viruses, these incomplete particles may play an important role in viral evolution.
Vyšlo v časopise:
Influenza Virus Reassortment Is Enhanced by Semi-infectious Particles but Can Be Suppressed by Defective Interfering Particles. PLoS Pathog 11(10): e32767. doi:10.1371/journal.ppat.1005204
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1005204
Souhrn
Since the genome of an influenza A virus has eight non-contiguous segments, two influenza A viruses can exchange genes readily when they infect the same cell. This process of reassortment is important to the evolution of the virus and is one reason why this pathogen is constantly changing. It has long been known that a large proportion of the virus particles that influenza and many other RNA viruses produce are not fully infectious, but the biological significance of these particles has remained unclear. Here we show that virus particles that deliver incomplete genomes to the cell enhance the rate of reassortment. Thus, despite their limited potential to produce progeny viruses, these incomplete particles may play an important role in viral evolution.
Zdroje
1. Palese P, Shaw ML (2006) Orthomyxoviridae: The Viruses and Their Replication. In: Knipe DMH, P. M., editor. Fields Virology. Philidelphia: Lippincott-Raven. pp. 1647–1690.
2. Palese P (1977) The genes of influenza virus. Cell 10: 1–10. 837439
3. Scholtissek C (1995) Molecular evolution of influenza viruses. Virus Genes 11: 209–215. 8828147
4. Steel J, Lowen AC (2014) Influenza A virus reassortment. Curr Top Microbiol Immunol 385: 377–401. doi: 10.1007/82_2014_395 25007845
5. Kilbourne ED (2006) Influenza pandemics of the 20th century. Emerg Infect Dis 12: 9–14. 16494710
6. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, et al. (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122–1125. doi: 10.1038/nature08182 19516283
7. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, et al. (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197–201. doi: 10.1126/science.1176225 19465683
8. Simonsen L, Viboud C, Grenfell BT, Dushoff J, Jennings L, et al. (2007) The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol Biol Evol 24: 1811–1820. 17522084
9. Holmes EC, Ghedin E, Miller N, Taylor J, Bao Y, et al. (2005) Whole-genome analysis of human influenza A virus reveals multiple persistent lineages and reassortment among recent H3N2 viruses. PLoS Biol 3: e300. 16026181
10. Westgeest KB, Russell CA, Lin X, Spronken MIJ, Bestebroer TM, et al. (2013) Genome-wide Analysis of Reassortment and Evolution of Human Influenza A(H3N2) Viruses Circulating between 1968 and 2011. Journal of Virology.
11. Nelson MI, Viboud C, Simonsen L, Bennett RT, Griesemer SB, et al. (2008) Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog 4: e1000012. doi: 10.1371/journal.ppat.1000012 18463694
12. Ince WL, Gueye-Mbaye A, Bennink JR, Yewdell JW (2013) Reassortment complements spontaneous mutation in influenza A virus NP and M1 genes to accelerate adaptation to a new host. J Virol 87: 4330–4338. doi: 10.1128/JVI.02749-12 23365443
13. Wei Z, McEvoy M, Razinkov V, Polozova A, Li E, et al. (2007) Biophysical characterization of influenza virus subpopulations using field flow fractionation and multiangle light scattering: correlation of particle counts, size distribution and infectivity. J Virol Methods 144: 122–132. 17586059
14. Enami M, Sharma G, Benham C, Palese P (1991) An influenza virus containing nine different RNA segments. Virology 185: 291–298. 1833874
15. Donald HB, Isaacs A (1954) Counts of influenza virus particles. J Gen Microbiol 10: 457–464. 13174769
16. Noton SL, Simpson-Holley M, Medcalf E, Wise HM, Hutchinson EC, et al. (2009) Studies of an influenza A virus temperature-sensitive mutant identify a late role for NP in the formation of infectious virions. J Virol 83: 562–571. doi: 10.1128/JVI.01424-08 18987140
17. 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 (Pt 6): 1415–1419. 3385408
18. Brooke CB (2014) Biological activities of 'noninfectious' influenza A virus particles. Future Virol 9: 41–51. 25067941
19. 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. doi: 10.1128/JVI.02680-08 19494019
20. Nayak DP, Tobita K, Janda JM, Davis AR, De BK (1978) Homologous interference mediated by defective interfering influenza virus derived from a temperature-sensitive mutant of influenza virus. J Virol 28: 375–386. 702654
21. Crumpton WM, Dimmock NJ, Minor PD, Avery RJ (1978) The RNAs of defective-interfering influenza virus. Virology 90: 370–373. 726256
22. Von Magnus P (1951) Propagation of the PR8 strain of influenza A virus in chick embryos. III. Properties of the incomplete virus produced in serial passages of undiluted virus. Acta Pathol Microbiol Scand 29: 157–181. 14902470
23. Von Magnus P (1951) Propagation of the PR8 strain of influenza A virus in chick embryos. II. The formation of incomplete virus following inoculation of large doses of seed virus. Acta Pathol Microbiol Scand 28: 278–293. 14856732
24. Parvin JD, Moscona A, Pan WT, Leider JM, Palese P (1986) Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1. J Virol 59: 377–383. 3016304
25. Drake JW (1993) Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A 90: 4171–4175. 8387212
26. Hirst GK (1973) Mechanism of influenza recombination. I. Factors influencing recombination rates between temperature-sensitive mutants of strain WSN and the classification of mutants into complementation—recombination groups. Virology 55: 81–93. 4738051
27. Brooke CB, Ince WL, Wrammert J, Ahmed R, Wilson PC, et al. (2013) Most influenza a virions fail to express at least one essential viral protein. J Virol 87: 3155–3162. doi: 10.1128/JVI.02284-12 23283949
28. Henle W, Liu OC (1951) Studies on host-virus interactions in the chick embryo-influenza virus system. VI. Evidence for multiplicity reactivation of inactivated virus. J Exp Med 94: 305–322. 14888814
29. Hirst GK, Pons MW (1973) Mechanism of influenza recombination. II. Virus aggregation and its effect on plaque formation by so-called noninfective virus. Virology 56: 620–631. 4796550
30. Marshall N, Priyamvada L, Ende Z, Steel J, Lowen AC (2013) Influenza virus reassortment occurs with high frequency in the absence of segment mismatch. PLoS Pathog 9: e1003421. doi: 10.1371/journal.ppat.1003421 23785286
31. Neumann G, Watanabe T, Kawaoka Y (2000) Plasmid-driven formation of influenza virus-like particles. J Virol 74: 547–551. 10590147
32. Weber M, Sediri H, Felgenhauer U, Binzen I, Banfer S, et al. (2015) Influenza virus adaptation PB2-627K modulates nucleocapsid inhibition by the pathogen sensor RIG-I. Cell Host Microbe 17: 309–319. doi: 10.1016/j.chom.2015.01.005 25704008
33. Ohkuma S, Poole B (1978) Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A 75: 3327–3331. 28524
34. Condit RC (2013) Principles of Virology. In: Knipe DM, Howley PM, editors. Fields Virology. 6th ed. pp. 21–51.
35. Davis AR, Hiti AL, Nayak DP (1980) Influenza defective interfering viral RNA is formed by internal deletion of genomic RNA. Proc Natl Acad Sci U S A 77: 215–219. 6928614
36. Nayak DP, Sivasubramanian N, Davis AR, Cortini R, Sung J (1982) Complete sequence analyses show that two defective interfering influenza viral RNAs contain a single internal deletion of a polymerase gene. Proc Natl Acad Sci U S A 79: 2216–2220. 6954536
37. Jonges M, Welkers MR, Jeeninga RE, Meijer A, Schneeberger P, et al. (2014) Emergence of the virulence-associated PB2 E627K substitution in a fatal human case of highly pathogenic avian influenza virus A(H7N7) infection as determined by Illumina ultra-deep sequencing. J Virol 88: 1694–1702. doi: 10.1128/JVI.02044-13 24257603
38. Saira K, Lin X, DePasse JV, Halpin R, Twaddle A, et al. (2013) Sequence analysis of in vivo defective interfering-like RNA of influenza A H1N1 pandemic virus. J Virol 87: 8064–8074. doi: 10.1128/JVI.00240-13 23678180
39. Janda JM, Nayak DP (1979) Defective influenza viral ribonucleoproteins cause interference. J Virol 32: 697–702. 501805
40. Nayak DP (1980) Defective interfering influenza viruses. Annu Rev Microbiol 34: 619–644. 7002033
41. Rott R, Scholtissek C (1963) Investigations About the Formation of Incomplete Forms of Fowl Plague Virus. J Gen Microbiol 33: 303–312. 14121206
42. Janda JM, Davis AR, Nayak DP, De BK (1979) Diversity and generation of defective interfering influenza virus particles. Virology 95: 48–58. 442544
43. Von Magnus P (1954) Incomplete forms of influenza virus. Adv Virus Res 2: 59–79. 13228257
44. Nayak DP, Chambers TM, Akkina RK (1985) Defective-interfering (DI) RNAs of influenza viruses: origin, structure, expression, and interference. Curr Top Microbiol Immunol 114: 103–151. 3888540
45. Duhaut SD, McCauley JW (1996) Defective RNAs inhibit the assembly of influenza virus genome segments in a segment-specific manner. Virology 216: 326–337. 8607262
46. Andino R, Domingo E (2015) Viral quasispecies. Virology.
47. Carter MJ, Mahy BW (1982) Incomplete avian influenza A virus displays anomalous interference. Arch Virol 74: 71–76. 7159221
48. Odagiri T, Tashiro M (1997) Segment-specific noncoding sequences of the influenza virus genome RNA are involved in the specific competition between defective interfering RNA and its progenitor RNA segment at the virion assembly step. J Virol 71: 2138–2145. 9032347
49. 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. doi: 10.1128/JVI.03193-13 24574404
50. Akkina RK, Chambers TM, Nayak DP (1984) Expression of defective-interfering influenza virus-specific transcripts and polypeptides in infected cells. J Virol 51: 395–403. 6205168
51. Odagiri T, Tominaga K, Tobita K, Ohta S (1994) An amino acid change in the non-structural NS2 protein of an influenza A virus mutant is responsible for the generation of defective interfering (DI) particles by amplifying DI RNAs and suppressing complementary RNA synthesis. J Gen Virol 75 (Pt 1): 43–53. 8113739
52. Tao H, Steel J, Lowen AC (2014) Intra-host dynamics of influenza virus reassortment. J Virol.
53. Tao H, Li L, White MC, Steel J, Lowen AC (2015) Influenza A virus co-infection through transmission can support high levels of reassortment. J Virol.
54. Brooke CB, Ince WL, Wei J, Bennink JR, Yewdell JW (2014) Influenza A virus nucleoprotein selectively decreases neuraminidase gene-segment packaging while enhancing viral fitness and transmissibility. Proc Natl Acad Sci U S A 111: 16854–16859. doi: 10.1073/pnas.1415396111 25385602
55. Chou YY, Vafabakhsh R, Doganay S, Gao Q, Ha T, et al. (2012) One influenza virus particle packages eight unique viral RNAs as shown by FISH analysis. Proc Natl Acad Sci U S A 109: 9101–9106. doi: 10.1073/pnas.1206069109 22547828
56. Noda T, Sagara H, Yen A, Takada A, Kida H, et al. (2006) Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 439: 490–492. 16437116
57. Noda T, Sugita Y, Aoyama K, Hirase A, Kawakami E, et al. (2012) Three-dimensional analysis of ribonucleoprotein complexes in influenza A virus. Nat Commun 3: 639. doi: 10.1038/ncomms1647 22273677
58. Chou YY, Heaton NS, Gao Q, Palese P, Singer R, et al. (2013) 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. doi: 10.1371/journal.ppat.1003358 23671419
59. Sugita Y, Sagara H, Noda T, Kawaoka Y (2013) Configuration of viral ribonucleoprotein complexes within the influenza A virion. J Virol 87: 12879–12884. doi: 10.1128/JVI.02096-13 24067952
60. Abraham G (1979) The effect of ultraviolet radiation on the primary transcription of influenza virus messenger RNAs. Virology 97: 177–182. 473590
61. Steel J, Lowen AC, Mubareka S, Palese P (2009) Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5: e1000252. doi: 10.1371/journal.ppat.1000252 19119420
62. Langley WA, Bradley KC, Li ZN, Smith ME, Schnell MJ, et al. (2010) Induction of neutralizing antibody responses to anthrax protective antigen by using influenza virus vectors: implications for disparate immune system priming pathways. J Virol 84: 8300–8307. doi: 10.1128/JVI.00183-10 20504926
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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