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Genetic Diversity and Evolution

Epochal Evolution of GGII.4 Norovirus Capsid Proteins from 1995 to 2006

J. Joukje Siebenga, Harry Vennema, Bernadet Renckens, Erwin de Bruin, Bas van der Veer, Roland J. Siezen, Marion Koopmans
J. Joukje Siebenga
1National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands
2Erasmus Medical Center, Rotterdam, The Netherlands
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  • For correspondence: Joukje.Siebenga@RIVM.nl
Harry Vennema
1National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands
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Bernadet Renckens
3Centre for Molecular and Biomolecular Informatics, Radboud University Medical Center, Nijmegen, The Netherlands
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Erwin de Bruin
1National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands
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Bas van der Veer
1National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands
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Roland J. Siezen
3Centre for Molecular and Biomolecular Informatics, Radboud University Medical Center, Nijmegen, The Netherlands
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Marion Koopmans
1National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands
2Erasmus Medical Center, Rotterdam, The Netherlands
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DOI: 10.1128/JVI.00674-07
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  • FIG. 1.
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    FIG. 1.

    MST, based on alignment of 145 nucleotides of the polymerase gene sequences (region A) of all GGII.4 strains found in The Netherlands between January 1995 and August 2006 (n = 574). Colors represent different variants, as indicated in the figure. The sizes of the circles are drawn to scale with their member counts. The smallest circles represent 1 strain, and the largest circle (the center of the 2002 cluster) represents 70 strains. Genetic distances between the circles, in numbers of nucleotides, are given on connecting lines. The total distance is 230 nucleotides. Strains included in this study are indicated. The strains shown as circles with dotted lines are considered outliers.

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    FIG. 2.

    Neighbor-joining tree for complete capsid amino acid sequences. Type strains from GenBank were used in order to emphasize and confirm the groupings. Branch lengths are drawn to scale. Bootstrap values are percentages of 1,000 iterations.

  • FIG. 3.
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    FIG. 3.

    Fixed amino acid changes (informative sites) in capsid sequences of GGII.4 outbreak strains collected between 1995 and 2006. The informative sites throughout the protein are listed from left to right. Amino acid numbering is indicated at the top, and outbreak dates (month-year of isolation, e.g., 01-95 is January 1995) and names are given on the left. From top to bottom, the same color indicates identical amino acids, and different colors are distinct amino acids. Colors were assigned by frequency; amino acids that occurred most are shown in green, followed by red, blue, and yellow (diminishing frequencies). The amino acids circled in magenta are part of the additional RGD motif present in the 2002 variant and the earliest strain. The arrow at the top indicates where an amino acid insertion occurred. The orange bars at the bottom indicate the locations of insertions in GGII.4 compared to NV and correspond to insertions 1 to 3 in Fig. 5A. Asterisks indicate hypervariable sites (with more than one mutation), and the arrows below the sequences indicate the sites where an amino acid mutation occurs at each variant change (not including 2006a). Domains are indicated in the bar below the figure.

  • FIG. 4.
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    FIG. 4.

    Graph showing the prevalence of GGII.4 variant types in The Netherlands between January 1995 and February 2007. Genotype and variant type assignments were done based on partial polymerase sequence data (region A) available from the Dutch norovirus surveillance database.

  • FIG. 5.
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    FIG. 5.

    Informative sites mapped on 3D model of GGII.4 capsid proteins. Sites with two distinct amino acid changes over the 12-year period are depicted in green, and sites with three or more amino acid changes are shown in red. The conserved RGD motif is shown in blue. (A) Dimeric subunit of two capsids, with one in gray and one in light blue. The extra RGD motif is indicated in yellow. The locations of the insertions compared to the NV capsid, which have not been modeled, are indicated by orange arrows 1 to 4. The brackets on the right indicate the different domains. The shell domain is indicated in grey, the P1 domain is shown in green, and the P2 domain is shown in blue. (B) Three capsid proteins, including a dimer with one-half of a neighboring dimer. The gray and light blue areas form one dimer, and the yellow capsid belongs to another dimer. The inserted RGD motif is indicated by the blue arrows.

  • FIG. 6.
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    FIG. 6.

    (A) (i to v) Changes in informative sites (green) derived from amino acid comparisons between subsequent epidemic variants. For each comparison, two views of the capsid protein are given, with one frontal view and one from the rear. For the 2006b variant, two comparisons were made, with the phylogenetic precursor (2002) and the chronologic precursor (2004). (B) Amino acids that change between every subsequent variant group, with 2006a not included.

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  • TABLE 1.

    Informative sites in GGII.4 capsid sequencesa

    Domainaa levelnt level
    aa positionsTotal length (aa)No. (%) of informative aant positionsTotal length (nt)No. (%) of informative ntNo. (%) of mutations at codon positionNo. (%) of silent mutationsNo. (%) of replacement mutations
    FirstSecondThird
    N-terminal domain1-40403 (8)1-12012010 (8)2 (20)2 (20)6 (60)7 (70)3 (30)
    S41-2221824 (2)121-66654670 (13)8 (11)2 (3)60 (86)66 (94)4 (6)
    P1223-276, 402-53118410 (5)667-828, 1204-159355291 (16)17 (19)5 (5)69 (76)75 (82)16 (18)
    P2227-40112530 (24)829-120337590 (24)18 (20)20 (22)52 (58)50 (56)40 (44)
    C-terminal domain531-541101 (10)1593-1623306 (20)1 (17)0 (0)5 (83)5 (83)1 (17)
    Total54148 (9)1623267 (16)46 (3)29 (2)192 (12)20364
    • ↵ a Percentages for informative sites are given as fractions of the total domain length, in numbers of amino acids or nucleotides. Position numbers are given for GGII.4 strains. aa, amino acid(s); nt, nucleotide(s).

Additional Files

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    Files in this Data Supplement:

    • Supplemental file 1 - Fig. S1 (Alignment of full RNA sequences of GGII.4 strains included in this study.)
      MS Word document, 531K.
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Epochal Evolution of GGII.4 Norovirus Capsid Proteins from 1995 to 2006
J. Joukje Siebenga, Harry Vennema, Bernadet Renckens, Erwin de Bruin, Bas van der Veer, Roland J. Siezen, Marion Koopmans
Journal of Virology Aug 2007, 81 (18) 9932-9941; DOI: 10.1128/JVI.00674-07

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Epochal Evolution of GGII.4 Norovirus Capsid Proteins from 1995 to 2006
J. Joukje Siebenga, Harry Vennema, Bernadet Renckens, Erwin de Bruin, Bas van der Veer, Roland J. Siezen, Marion Koopmans
Journal of Virology Aug 2007, 81 (18) 9932-9941; DOI: 10.1128/JVI.00674-07
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KEYWORDS

amino acid substitution
Capsid Proteins
Evolution, Molecular
genetic drift
Norwalk virus
Selection, Genetic

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