Rapid Evolution of Pandemic Noroviruses of the GII.4 Lineage
Over the last fifteen years there have been five pandemics of norovirus (NoV) associated gastroenteritis, and the period of stasis between each pandemic has been progressively shortening. NoV is classified into five genogroups, which can be further classified into 25 or more different human NoV genotypes; however, only one, genogroup II genotype 4 (GII.4), is associated with pandemics. Hence, GII.4 viruses have both a higher frequency in the host population and greater epidemiological fitness. The aim of this study was to investigate if the accuracy and rate of replication are contributing to the increased epidemiological fitness of the GII.4 strains. The replication and mutation rates were determined using in vitro RNA dependent RNA polymerase (RdRp) assays, and rates of evolution were determined by bioinformatics. GII.4 strains were compared to the second most reported genotype, recombinant GII.b/GII.3, the rarely detected GII.3 and GII.7 and as a control, hepatitis C virus (HCV). The predominant GII.4 strains had a higher mutation rate and rate of evolution compared to the less frequently detected GII.b, GII.3 and GII.7 strains. Furthermore, the GII.4 lineage had on average a 1.7-fold higher rate of evolution within the capsid sequence and a greater number of non-synonymous changes compared to other NoVs, supporting the theory that it is undergoing antigenic drift at a faster rate. Interestingly, the non-synonymous mutations for all three NoV genotypes were localised to common structural residues in the capsid, indicating that these sites are likely to be under immune selection. This study supports the hypothesis that the ability of the virus to generate genetic diversity is vital for viral fitness.
Vyšlo v časopise:
Rapid Evolution of Pandemic Noroviruses of the GII.4 Lineage. PLoS Pathog 6(3): e32767. doi:10.1371/journal.ppat.1000831
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000831
Souhrn
Over the last fifteen years there have been five pandemics of norovirus (NoV) associated gastroenteritis, and the period of stasis between each pandemic has been progressively shortening. NoV is classified into five genogroups, which can be further classified into 25 or more different human NoV genotypes; however, only one, genogroup II genotype 4 (GII.4), is associated with pandemics. Hence, GII.4 viruses have both a higher frequency in the host population and greater epidemiological fitness. The aim of this study was to investigate if the accuracy and rate of replication are contributing to the increased epidemiological fitness of the GII.4 strains. The replication and mutation rates were determined using in vitro RNA dependent RNA polymerase (RdRp) assays, and rates of evolution were determined by bioinformatics. GII.4 strains were compared to the second most reported genotype, recombinant GII.b/GII.3, the rarely detected GII.3 and GII.7 and as a control, hepatitis C virus (HCV). The predominant GII.4 strains had a higher mutation rate and rate of evolution compared to the less frequently detected GII.b, GII.3 and GII.7 strains. Furthermore, the GII.4 lineage had on average a 1.7-fold higher rate of evolution within the capsid sequence and a greater number of non-synonymous changes compared to other NoVs, supporting the theory that it is undergoing antigenic drift at a faster rate. Interestingly, the non-synonymous mutations for all three NoV genotypes were localised to common structural residues in the capsid, indicating that these sites are likely to be under immune selection. This study supports the hypothesis that the ability of the virus to generate genetic diversity is vital for viral fitness.
Zdroje
1. EstesMK
PrasadBV
AtmarRL
2006 Noroviruses everywhere: has something changed? Curr Opin Infect Dis 19 467 474
2. ElenaSF
SanjuanR
2005 Adaptive value of high mutation rates of RNA viruses: separating causes from consequences. J Virol 79 11555 11558
3. ManrubiaSC
EscarmisC
DomingoE
LazaroE
2005 High mutation rates, bottlenecks, and robustness of RNA viral quasispecies. Gene 347 273 282
4. LindesmithLC
DonaldsonEF
LobueAD
CannonJL
ZhengDP
2008 Mechanisms of GII.4 Norovirus Persistence in Human Populations. PLoS Med 5 e31 doi:10.1371/journal.pmed.0050031
5. DomingoE
EscarmisC
SevillaN
MoyaA
ElenaSF
1996 Basic concepts in RNA virus evolution. Faseb J 10 859 864
6. AtmarRL
EstesMK
2001 Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin Microbiol Rev 14 15 37
7. GreenKY
ChanockRM
KapikianAZ
2001 Human calicivirus.
KDM
HPM
Fields virology. 4 ed Philadelphia Lippincott Williams & Wilkins 841 874
8. GlassPJ
WhiteLJ
BallJM
Leparc-GoffartI
HardyME
2000 Norwalk virus open reading frame 3 encodes a minor structural protein. J Virol 74 6581 6591
9. PletnevaMA
SosnovtsevSV
GreenKY
2001 The genome of hawaii virus and its relationship with other members of the caliciviridae. Virus Genes 23 5 16
10. ZhengDP
AndoT
FankhauserRL
BeardRS
GlassRI
2006 Norovirus classification and proposed strain nomenclature. Virology 346 312 323
11. ChenR
NeillJD
NoelJS
HutsonAM
GlassRI
2004 Inter- and intragenus structural variations in caliciviruses and their functional implications. J Virol 78 6469 6479
12. PrasadBV
HardyME
DoklandT
BellaJ
RossmannMG
1999 X-ray crystallographic structure of the Norwalk virus capsid. Science 286 287 290
13. TanM
HegdeRS
JiangX
2004 The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J Virol 78 6233 6242
14. TanM
JiangX
2005 The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol 79 14017 14030
15. SiebengaJJ
VennemaH
RenckensB
de BruinE
van der VeerB
2007 Epochal Evolution of GGII.4 Norovirus Capsid Proteins from 1995 to 2006. J Virol
16. BullRA
TuET
McIverCJ
RawlinsonWD
WhitePA
2006 Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J Clin Microbiol 44 327 333
17. TuET
BullRA
GreeningGE
HewittJ
LyonMJ
2008 Epidemics of gastroenteritis during 2006 were associated with the spread of norovirus GII.4 variants 2006a and 2006b. Clin Infect Dis 46 413 420
18. DoyleTJ
StarkL
HammondR
HopkinsRS
2008 Outbreaks of noroviral gastroenteritis in Florida, 2006–2007. Epidemiol Infect: 1 9
19. SiebengaJJ
VennemaH
ZhengDP
VinjeJ
LeeBE
2009 Norovirus Illness Is a Global Problem: Emergence and Spread of Norovirus GII.4 Variants, 2001–2007. J Infect Dis 200 802 812
20. DomingoE
2007 Virus Evolution.
KnipeDM
HowleyPM
Field's Virology. 5th ed Philadelphia Lippincott Williams & Wilkins 389 422
21. HayAJ
GregoryV
DouglasAR
LinYP
2001 The evolution of human influenza viruses. Philos Trans R Soc Lond B Biol Sci 356 1861 1870
22. NobusawaE
SatoK
2006 Comparison of the mutation rates of human influenza A and B viruses. J Virol 80 3675 3678
23. DomingoE
HollandJJ
1997 RNA virus mutations and fitness for survival. Annu Rev Microbiol 51 151 178
24. HansmanGS
KatayamaK
ManeekarnN
PeerakomeS
KhamrinP
2004 Genetic diversity of norovirus and sapovirus in hospitalized infants with sporadic cases of acute gastroenteritis in Chiang Mai, Thailand. J Clin Microbiol 42 1305 1307
25. JonesLA
ClancyLE
RawlinsonWD
WhitePA
2006 High-affinity aptamers to subtype 3a hepatitis C virus polymerase display genotypic specificity. Antimicrob Agents Chemother 50 3019 3027
26. WardCD
StokesMA
FlaneganJB
1988 Direct measurement of the poliovirus RNA polymerase error frequency in vitro. J Virol 62 558 562
27. FergusonNM
GalvaniAP
BushRM
2003 Ecological and immunological determinants of influenza evolution. Nature 422 428 433
28. TamuraK
DudleyJ
NeiM
KumarS
2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599
29. PrideDT
BlaserMJ
2002 Concerted evolution between duplicated genetic elements in Helicobacter pylori. J Mol Biol 316 629 642
30. NeiM
GojoboriT
1986 Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3 418 426
31. LundO
NielsenM
LundegaardC
WorningP
2002 CPHmodels 2.0: X3M a Computer Program to Extract 3D Models. Critical Assessment of Techniques for Protein Structure Prediction (CASP5) Conference. California, United States
32. DeLanoWL
2002 The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA
33. DrakeJW
1993 Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A 90 4171 4175
34. BlantonLH
AdamsSM
BeardRS
WeiG
BulensSN
2006 Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000–2004. J Infect Dis 193 413 421
35. AllenDJ
GrayJJ
GallimoreCI
XerryJ
Iturriza-GomaraM
2008 Analysis of Amino Acid Variation in the P2 Domain of the GII-4 Norovirus VP1 Protein Reveals Putative Variant-Specific Epitopes. PLoS ONE 3 e1485 doi:10.1371/journal.pone.0001485
36. TanM
JiangX
2005 Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol 13 285 293
37. HalperinT
VennemaH
KoopmansM
Kahila Bar-GalG
KayoufR
2008 No Association between Histo-Blood Group Antigens and Susceptibility to Clinical Infections with Genogroup II Norovirus. J Infect Dis 197 63 65
38. ChoiJM
HutsonAM
EstesMK
PrasadBV
2008 Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc Natl Acad Sci U S A 105 9175 9180
39. LindesmithL
MoeC
LependuJ
FrelingerJA
TreanorJ
2005 Cellular and humoral immunity following Snow Mountain virus challenge. J Virol 79 2900 2909
40. PfeifferJK
KirkegaardK
2005 Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog 1 e11 doi:10.1371/journal.ppat.0010011
41. VignuzziM
WendtE
AndinoR
2008 Engineering attenuated virus vaccines by controlling replication fidelity. Nat Med 14 154 161
42. MontvilleR
FroissartR
RemoldSK
TenaillonO
TurnerPE
2005 Evolution of mutational robustness in an RNA virus. PLoS Biol 3 e381 doi:10.1371/journal.pbio.0030381
43. DomingoE
1997 Rapid evolution of viral RNA genomes. J Nutr 127 958S 961S
44. SallieR
2005 Replicative homeostasis: a fundamental mechanism mediating selective viral replication and escape mutation. Virol J 2 10
45. KunkelTA
SchaaperRM
BeckmanRA
LoebLA
1981 On the fidelity of DNA replication. Effect of the next nucleotide on proofreading. J Biol Chem 256 9883 9889
46. MondelliMU
CerinoA
LisaA
BrambillaS
SegagniL
1999 Antibody responses to hepatitis C virus hypervariable region 1: evidence for cross-reactivity and immune-mediated sequence variation. Hepatology 30 537 545
47. PhanTG
NguyenTA
NishimuraS
NishimuraT
YamamotoA
2005 Etiologic agents of acute gastroenteritis among Japanese infants and children: virus diversity and genetic analysis of sapovirus. Arch Virol 150 1415 1424
48. AndreoniM
2004 Viral phenotype and fitness. New Microbiol 27 71 76
49. BruennJA
2003 A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. Nucleic Acids Res 31 1821 1829
50. BoniMF
GogJR
AndreasenV
ChristiansenFB
2004 Influenza drift and epidemic size: the race between generating and escaping immunity. Theor Popul Biol 65 179 191
51. KumarS
TamuraK
NeiM
2004 MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5 150 163
52. CaoS
LouZ
TanM
ChenY
LiuY
2007 Structural basis for the recognition of blood group trisaccharides by norovirus. J Virol 81 5949 5957
53. RispeterK
LuM
BehrensSE
FumikoC
YoshidaT
2000 Hepatitis C virus variability: sequence analysis of an isolate after 10 years of chronic infection. Virus Genes 21 179 188
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 3
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Kaposi's Sarcoma-Associated Herpesvirus ORF57 Protein Binds and Protects a Nuclear Noncoding RNA from Cellular RNA Decay Pathways
- Endocytosis of the Anthrax Toxin Is Mediated by Clathrin, Actin and Unconventional Adaptors
- Perforin and IL-2 Upregulation Define Qualitative Differences among Highly Functional Virus-Specific Human CD8 T Cells
- Inhibition of Macrophage Migration Inhibitory Factor Ameliorates Ocular -Induced Keratitis