Structural and nonstructural genes contribute to the genetic diversity of RNA viruses

mBio

Volumn 9, Issue 5, 2018, Pages 1-13

  Collins, Natalie D ^a   Beck, Andrew S ^a   Widen, Steven G ^b   Wood, Thomas G ^b   Higgs, Stephen ^c   Barrett, Alan D T ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

Attenuation; Diversity; RNA viruses; Vaccine; Viral population; Yellow fever

Indexed keywords

VIRAL PROTEIN;

A-549 CELL LINE; GENETIC RECOMBINATION; GENETIC VARIATION; GENETICS; HUMAN; MUTATION RATE; REVERSE GENETICS; YELLOW FEVER VIRUS;

A549 CELLS; GENETIC VARIATION; HUMANS; MUTATION RATE; RECOMBINATION, GENETIC; REVERSE GENETICS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL STRUCTURAL PROTEINS; YELLOW FEVER VIRUS;

EID: 85055618969     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mbio.01871-18     Document Type: Article

References (56)

1. Monath TP. 2013. 17D yellow fever virus vaccine. Am J Trop Med Hyg 89:1225. https://doi.org/10.4269/ajtmh.13-0443a.
2. Norrby E. 2007. Yellow fever and Max Theiler: the only Nobel Prize for a virus vaccine. J Exp Med 204:2779–2784. https://doi.org/10.1084/jem.20072290.
3. Theiler M, Smith HH. 1937. The use of yellow fever virus modified by in vitro cultivation for human immunization. J Exp Med 65:787–800. https://doi.org/10.1084/jem.65.6.787.
4. Staples JE, Gershman M, Fischer M. 2010. Yellow fever vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 59:1–27.
5. Collins ND, Barrett AD. 2017. Live attenuated yellow fever 17D vaccine: a legacy vaccine still controlling outbreaks in modern day. Curr Infect Dis Rep 19:14. https://doi.org/10.1007/s11908-017-0566-9.
6. Barrett AD, Higgs S. 2007. Yellow fever: a disease that has yet to be conquered. Annu Rev Entomol 52:209–229. https://doi.org/10.1146/annurev.ento.52.110405.091454.
7. Beasley DW, McAuley AJ, Bente DA. 2015. Yellow fever virus: genetic and phenotypic diversity and implications for detection, prevention and therapy. Antiviral Res 115:48–70. https://doi.org/10.1016/j.antiviral.2014.12.010.
8. Lauring AS, Andino R. 2010. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 6:e1001005. https://doi.org/10.1371/journal.ppat.1001005.
9. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 2006. Quasispe-cies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–348. https://doi.org/10.1038/nature04388.
10. Beck A, Tesh RB, Wood TG, Widen SG, Ryman KD, Barrett AD. 2014. Comparison of the live attenuated yellow fever vaccine 17D-204 strain to its virulent parental strain Asibi by deep sequencing. J Infect Dis 209:334–344. https://doi.org/10.1093/infdis/jit546.
11. Salmona M, Gazaigne S, Mercier-Delarue S, Garnier F, Korimbocus J, Colin de Verdière N, LeGoff J, Roques P, Simon F. 2015. Molecular characterization of the 17D-204 yellow fever vaccine. Vaccine 33: 5432–5436. https://doi.org/10.1016/j.vaccine.2015.08.055.
12. Pugachev KV, Guirakhoo F, Ocran SW, Mitchell F, Parsons M, Penal C, Girakhoo S, Pougatcheva SO, Arroyo J, Trent DW, Monath TP. 2004. High fidelity of yellow fever virus RNA polymerase. J Virol 78:1032–1038. https://doi.org/10.1128/JVI.78.2.1032-1038.2004.
13. Dos Santos CN, Post PR, Carvalho R, Ferreira II, Rice CM, Galler R. 1995. Complete nucleotide sequence of yellow fever virus vaccine strains 17DD and 17D-213. Virus Res 35:35–41. https://doi.org/10.1016/0168-1702(94)00076-O.
14. Hahn CS, Dalrymple JM, Strauss JH, Rice CM. 1987. Comparison of the virulent Asibi strain of yellow fever virus with the 17D vaccine strain derived from it. Proc Natl Acad Sci USA84:2019–2023. https://doi.org/10.1073/pnas.84.7.2019.
15. Selisko B, Wang C, Harris E, Canard B. 2014. Regulation of flavivirus RNA synthesis and replication. Curr Opin Virol 9:74–83. https://doi.org/10.1016/j.coviro.2014.09.011.
16. Shi P-YY. 2014. Structural biology. Unraveling a flavivirus enigma. Science 343:849–850. https://doi.org/10.1126/science.1251249.
17. Khromykh AA, Sedlak PL, Westaway EG. 2000. cis-and trans-acting elements in flavivirus RNA replication. J Virol 74:3253–3263. https://doi.org/10.1128/JVI.74.7.3253-3263.2000.
18. Li K, Phoo WW, Luo D. 2014. Functional interplay among the flavivirus NS3 protease, helicase, and cofactors. Virol Sin 29:74–85. https://doi.org/10.1007/s12250-014-3438-6.
19. Li X-DD, Deng C-LL, Ye H-QQ, Zhang H-LL, Zhang Q-YY, Chen D-DD, Zhang P-TT, Shi P-YY, Yuan Z-MM, Zhang B. 2016. Transmembrane domains of NS2B contribute to both viral RNA replication and particle formation in Japanese encephalitis virus. J Virol 90:5735–5749. https://doi.org/10.1128/JVI.00340-16.
20. Li X-DD, Ye H-QQ, Deng C-LL, Liu S-QQ, Zhang H-LL, Shang B-DD, Shi P-YY, Yuan Z-MM, Zhang B. 2015. Genetic interaction between NS4A and NS4B for replication of Japanese encephalitis virus. J Gen Virol 96: 1264–1275. https://doi.org/10.1099/vir.0.000044.
21. Nemésio H, Palomares-Jerez F, Villalaín J. 2012. NS4A and NS4B proteins from dengue virus: membranotropic regions. Biochim Biophys Acta 1818:2818–2830. https://doi.org/10.1016/j.bbamem.2012.06.022.
22. Tajima S, Takasaki T, Kurane I. 2011. Restoration of replication-defective dengue type 1 virus bearing mutations in the N-terminal cytoplasmic portion of NS4A by additional mutations in NS4B. Arch Virol 156:63–69. https://doi.org/10.1007/s00705-010-0816-8.
23. Youn S, Li T, McCune B, Edeling M, Fremont D, Cristea I, Diamond M. 2012. Evidence for a genetic and physical interaction between nonstruc-tural proteins NS1 and NS4B that modulates replication of West Nile virus. J Virol 86:7360–7371. https://doi.org/10.1128/JVI.00157-12.
24. Zou J, Xie X, Wang Q-YY, Dong H, Lee MY, Kang C, Yuan Z, Shi P-YY. 2015. Characterization of dengue virus NS4A and NS4B protein interaction. J Virol 89:3455–3470. https://doi.org/10.1128/JVI.03453-14.
25. Zou J, Lee LTT, Wang QY, Xie X, Lu S, Yau YH, Yuan Z, Geifman Shochat S, Kang C, Lescar J, Shi P-YY. 2015. Mapping the interactions between the NS4B and NS3 proteins of dengue virus. J Virol 89:3471–3483. https://doi.org/10.1128/JVI.03454-14.
26. Green AM, Beatty PR, Hadjilaou A, Harris E. 2014. Innate immunity to dengue virus infection and subversion of antiviral responses. J Mol Biol 426:1148–1160. https://doi.org/10.1016/j.jmb.2013.11.023.
27. Jones M, Davidson A, Hibbert L, Gruenwald P, Schlaak J, Ball S, Foster GR, Jacobs M. 2005. Dengue virus inhibits alpha interferon signaling by reducing STAT2 expression. J Virol 79:5414–5420. https://doi.org/10.1128/JVI.79.9.5414-5420.2005.
28. Munoz-Jordan JL, Laurent-Rolle M, Ashour J, Martinez-Sobrido L, Ashok M, Lipkin WI, Garcia-Sastre A. 2005. Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J Virol 79:8004–8013. https://doi.org/10.1128/JVI.79.13.8004-8013.2005.
29. Grant D, Tan GK, Qing M, Ng JK, Yip A, Zou G, Xie X, Yuan Z, Schreiber MJ, Schul W, Shi P-YY, Alonso S. 2011. A single amino acid in nonstruc-tural protein NS4B confers virulence to dengue virus in AG129 mice through enhancement of viral RNA synthesis. J Virol 85:7775–7787. https://doi.org/10.1128/JVI.00665-11.
30. McElroy KL, Tsetsarkin KA, Vanlandingham DL, Higgs S. 2006. Manipu-lation of the yellow fever virus non-structural genes 2A and 4B and the 3’non-coding region to evaluate genetic determinants of viral dissemination from the Aedes aegypti midgut. Am J Trop Med Hyg 75: 1158–1164. https://doi.org/10.4269/ajtmh.2006.75.1158.
31. Yang X, Charlebois P, Macalalad A, Henn MR, Zody MC. 2013. V-Phaser 2: variant inference for viral populations. BMC Genomics 14:674. https://doi.org/10.1186/1471-2164-14-674.
32. McElroy KL, Tsetsarkin KA, Vanlandingham DL, Higgs S. 2006. Role of the yellow fever virus structural protein genes in viral dissemination from the Aedes aegypti mosquito midgut. J Gen Virol 87:2993–3001. https://doi.org/10.1099/vir.0.82023-0.
33. McElroy KL, Girard YA, McGee CE, Tsetsarkin KA, Vanlandingham DL, Higgs S. 2008. Characterization of the antigen distribution and tissue tropisms of three phenotypically distinct yellow fever virus variants in orally infected Aedes aegypti mosquitoes. Vector Borne Zoonotic Dis 8:675–687. https://doi.org/10.1089/vbz.2007.0269.
34. Lee E, Lobigs M. 2008. E protein domain III determinants of yellow fever virus 17D vaccine strain enhance binding to glycosaminoglycans, im-pede virus spread, and attenuate virulence. J Virol 82:6024–6033. https://doi.org/10.1128/JVI.02509-07.
35. Sanjuán R, Domingo-Calap P. 2016. Mechanisms of viral mutation. Cell Mol Life Sci 73:4433–4448. https://doi.org/10.1007/s00018-016-2299-6.
36. Borderia AV, Rozen-Gagnon K, Vignuzzi M. 2016. Fidelity variants and RNA quasispecies. Curr Top Microbiol Immunol 392:303–322.
37. Pfeiffer JK, Kirkegaard K. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog 1:e11. https://doi.org/10.1371/journal.ppat.0010011.
38. Pfeiffer JK, Kirkegaard K. 2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc Natl Acad Sci USA100:7289–7294. https://doi.org/10.1073/pnas.1232294100.
39. Korboukh VK, Lee CA, Acevedo A, Vignuzzi M, Xiao Y, Arnold JJ, Hemp-erly S, Graci JD, August A, Andino R, Cameron CE. 2014. RNA virus population diversity, an optimum for maximal fitness and virulence. J Biol Chem 289:29531–29544. https://doi.org/10.1074/jbc.M114.592303.
40. Coffey LL, Vignuzzi M. 2011. Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. J Virol 85:1025–1035. https://doi.org/10.1128/JVI.01918-10.
41. Coffey LL, Beeharry Y, Bordería AV, Blanc H, Vignuzzi M. 2011. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad SciUSA108:16038–16043. https://doi.org/10.1073/pnas.1111650108.
42. Rozen-Gagnon K, Stapleford KA, Mongelli V, Blanc H, Failloux A-BB, Saleh M-CC, Vignuzzi M. 2014. Alphavirus mutator variants present host-specific defects and attenuation in mammalian and insect models. PLoS Pathog 10:e1003877. https://doi.org/10.1371/journal.ppat.1003877.
43. Van Slyke GA, Arnold JJ, Lugo AJ, Griesemer SB, Moustafa IM, Kramer LD, Cameron CE, Ciota AT. 2015. Sequence-specific fidelity alterations associated with West Nile virus attenuation in mosquitoes. PLoS Pathog 11:e1005009. https://doi.org/10.1371/journal.ppat.1005009.
44. Xie X, Wang H, Zeng J, Li C, Zhou G, Yang D, Yu L. 2014. Foot-and-mouth disease virus low-fidelity polymerase mutants are attenuated. Arch Virol 159:2641–2650. https://doi.org/10.1007/s00705-014-2126-z.
45. Zeng J, Wang H, Xie X, Yang D, Zhou G, Yu L. 2013. An increased replication fidelity mutant of foot-and-mouth disease virus retains fitness in vitro and virulence in vivo. Antiviral Res 100:1–7. https://doi.org/10.1016/j.antiviral.2013.07.008.
46. Zeng J, Wang H, Xie X, Li C, Zhou G, Yang D, Yu L. 2014. Ribavirin-resistant variants of foot-and-mouth disease virus: the effect of restricted quasispecies diversity on viral virulence. J Virol 88:4008–4020. https://doi.org/10.1128/JVI.03594-13.
47. Xie H, Cass AR, Barrett AD. 1998. Yellow fever 17D vaccine virus isolated from healthy vaccinees accumulates very few mutations. Virus Res 55: 93–99. https://doi.org/10.1016/S0168-1702(98)00036-7.
48. Tangy F, Desprès P. 2014. Yellow fever vaccine attenuation revealed: loss of diversity. J Infect Dis 209:318–320. https://doi.org/10.1093/infdis/jit551.
49. Sim S, Aw PP, Wilm A, Teoh G, Hue KD, Nguyen NM, Nagarajan N, Simmons CP, Hibberd ML. 2015. Tracking dengue virus intra-host genetic diversity during human-to-mosquito transmission. PLoS Negl Trop Dis 9:e0004052. https://doi.org/10.1371/journal.pntd.0004052.
50. Sessions OM, Wilm A, Kamaraj US, Choy MM, Chow A, Chong Y, Ong XM, Nagarajan N, Cook AR, Ooi EE. 2015. Analysis of dengue virus genetic diversity during human and mosquito infection reveals genetic con-straints. PLoS Negl Trop Dis 9:e0004044. https://doi.org/10.1371/journal.pntd.0004044.
51. Grubaugh ND, Rückert C, Armstrong PM, Bransfield A, Anderson JF, Ebel GD, Brackney DE. 2016. Transmission bottlenecks and RNAi collectively influence tick-borne flavivirus evolution. Virus Evol 2:vew033. https://doi.org/10.1093/ve/vew033.
52. Lequime S, Richard V, Cao-Lormeau V-MM, Lambrechts L. 2017. Full-genome dengue virus sequencing in mosquito saliva shows lack of convergent positive selection during transmission by Aedes aegypti. Virus Evol 3:vex031. https://doi.org/10.1093/ve/vex031.
53. Grubaugh ND, Weger-Lucarelli J, Murrieta RA, Fauver JR, Garcia-Luna SM, Prasad AN, Black WC, Ebel GD. 2016. Genetic drift during systemic arbovirus infection of mosquito vectors leads to decreased relative fitness during host switching. Cell Host Microbe 19:481–492. https://doi.org/10.1016/j.chom.2016.03.002.
54. Dudley DM, Newman CM, Lalli J, Stewart LM, Koenig MR, Weiler AM, Semler MR, Barry GL, Zarbock KR, Mohns MS, Breitbach ME, Schultz-Darken N, Peterson E, Newton W, Mohr EL, Capuano S, III, Osorio JE, O’Connor SL, O’Connor DH, Friedrich TC, Aliota MT. 2017. Infection via mosquito bite alters Zika virus tissue tropism and replication kinetics in rhesus macaques. Nat Commun 8:2096. https://doi.org/10.1038/s41467-017-02222-8.
55. Acevedo A, Brodsky L, Andino R. 2014. Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 505: 686–690. https://doi.org/10.1038/nature12861.
56. Nishijima N, Marusawa H, Ueda Y, Takahashi K, Nasu A, Osaki Y, Kou T, Yazumi S, Fujiwara T, Tsuchiya S, Shimizu K, Uemoto S, Chiba T. 2012. Dynamics of hepatitis B virus quasispecies in association with nucleos-(t)ide analogue treatment determined by ultra-deep sequencing. PLoS One 7:e35052. https://doi.org/10.1371/journal.pone.0035052.