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: 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

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