Genetic variation in the VP7 gene of rot

Virus Research 165 (2012) 190–196 Contents lists available at SciVerse ScienceDirect Virus Research journal homepage: www.elsevier.com/locate/virusres Genetic variation in the VP7 gene of rotavirus G1P[8] strains isolated in Vietnam, 1998–2009 Nguyen Van Trang a , Tetsu Yamashiro b,c , Le Thi Kim Anh a , Vu Thi Bich Hau a , Le Thi Luan d , Dang Duc Anh a,∗ a The National Institute of Hygiene and Epidemiology, Ha Noi, Viet Nam Center for Infectious Disease Research in Asia and Africa, Institute of Tropical Medicine, Nagasaki University, Japan c Vietnam Research Station, Japan Initiative for Global Research Network on Infectious Diseases (J-GRID), Ha Noi, Viet Nam d Center for Research and Production of Vaccines and Biologicals, Ha Noi, Viet Nam b a r t i c l e i n f o Article history: Received 17 October 2011 Received in revised form February 2012 Accepted 16 February 2012 Available online 25 February 2012 Keywords: Rotavirus G1P[8] VP7 Genetic variation Vietnam a b s t r a c t Group A rotavirus genotype G1P[8] is the most common strain affecting humans around the world over the past few decades In this study, we examined genetic variation in the VP7 gene of rotavirus G1P[8] strains, detected in children of four major cities of Vietnam during three different rotavirus seasons: 1998–1999, 2007–2008 and 2008–2009 in order to assess the evolution of the virus over 11 years Fecal samples (n = 73) from children hospitalized for gastroenteritis caused by G1P[8] rotavirus were analyzed by DNA sequencing of gene encoding the VP7 capsid protein Phylogenetic analyses indicated that VP7 gene of the G1 strains from 1999 contained a lineage I, while rotaviruses from 2009 clustered in lineage II Both of these lineages were found co-circulating in 2007–2008 season While different sublineages of lineage I and II co-circulated in the 1998–1999 and 2007–2008 seasons, almost all strains in 2009 belonged to sub-lineage II-C In the analysis using selected 10 strains, the VP4 genes of these VP7-G1 lineages were all grouped in F45-like cluster Deduced amino acid analyses indicated that there were thirteen amino acid substitutions between strains of two lineages Of those, two were found in antigenic regions A and C, implying possible antigenic differences between these two lineages The G1P[8] strains in Vietnam are very genetically diverse and dynamic, implying the frequent monitoring on evolution of rotavirus will be important to assess efficacy of rotavirus vaccine in Vietnam © 2012 Elsevier B.V All rights reserved Introduction Rotavirus is the most important cause of acute gastroenteritis (AGE) in children worldwide In Vietnam, rotavirus is responsible for more than 50% of AGE cases in hospitalized children (Van Man et al., 2005) Rotaviruses which form a genus of the Reoviridae family, are non-enveloped virus with 11 segments of double stranded RNA as their genome The VP4 and VP7 proteins of the outer capsid encoded by gene segments and 9, respectively, are important neutralizing antigens and define independent G and P serotype specificities (Kapikian et al., 2001) There are now 27 G and 35 P types described in human and animals (Matthijnssens et al., 2011) Much like cases of influenza virus, seasonal shifts of group A rotavirus strains have been contributing to the persistence of the virus in a human population (Parra, 2009) In addition, genetic drift is implied by the presence and emergence of different lineages ∗ Corresponding author at: The National Institute of Hygiene and Epidemiology, No Yersin Street, Ha Noi, Viet Nam Tel.: +84 43 971 2989; fax: +84 43 821 2660 E-mail address: ducanhnihe@hn.vnn.vn (D.D Anh) 0168-1702/$ – see front matter © 2012 Elsevier B.V All rights reserved doi:10.1016/j.virusres.2012.02.015 within a genotype Almost all genotypes have different lineages, genotype G9 has at least lineages (Hoshino et al., 2004), genotype G2 has at least lineages, genotype G4 has lineages and several sublineages (Trinh et al., 2010) Genotype G1P[8] has been reported as the most common rotavirus strain circulating around the world, accounting for 53% of all rotavirus genotypes (Gentsch et al., 2005; Santos and Hoshino, 2005) The diversity within genotype G1 is great; 11 different lineages and 17 sublineages have been described (Phan et al., 2007) Phan et al proposed an identification method based on signature codes consisted of 14 amino acids at positions 29, 34, 35, 37, 42, 43, 50, 55, 57, 65, 68, 72, 74 and 75 in the VP7 region of G1 rotavirus that define phylogenetic lineages and sub-lineages of the G1 genotype The code for lineage I is IIYFVAALITSQ(R)G(E)V, for lineage III is IIYFVAALLATQEV and for lineage XI is MIYFVTAILTAKET Further modifications in this code identified sublineages of G1 rotavirus In this study we used this identification code to study changes in genotype G1 lineages of strains from different regions in Vietnam In Vietnam, G1[8] had been the dominant strain until 2005 with a prevalence of 58.3% (Van Man et al., 2005) After a brief period of the dominance with G3 rotavirus in 2006–2009 (Ngo et al., 2009), N.V Trang et al / Virus Research 165 (2012) 190–196 Table Number of rotavirus analyzed in this study Site of sample collection Season 1998–1999a North of Vietnam Hanoi Haiphong South of Vietnam Nha Trang Ho Chi Minh city Total 2007–2008a 7 19 10 28 2008–2009a b NA 10 26 a The total numbers of G1P[8] strains detected in 2007–2008 and 2008–2009 seasons were 181 and 256 samples, respectively Genotypings were not performed in all samples of 1998–1999 season, so the total number of G1P[8] strains in this season was not determined b NA: samples not collected in this site at this time point G1P[8] strains returned in 2010 (Nguyen Van Trang et al., unpublished data) One G1P[8] strain has been chosen as the candidate for vaccine in Vietnam, even though the diversity of the G1P[8] rotavirus has not been well studied Considering the large genetic diversity of G1P[8] rotavirus in particular, it raises a concern that accumulation of point mutations in antigenic regions of VP7 and VP4 gene could result in rotavirus strains that are less effective by vaccine induced neutralizing antibodies and overtime would result in predominance of rotavirus strains which are less effected by or even resistant to the vaccine (Matthijnssens et al., 2009) Among the lineages of G9P[8], it is recommended that lineage should be included in the vaccine since antisera developed to this lineage could neutralize the other lineages efficiently whereas antisera to either lineage and could not neutralize other lineages efficiently (Hoshino et al., 2004) In this study, we examined mutations in gene (VP7) of G1P[8] strains isolated in four major cities of Vietnam in three different periods between 1999 and 2009 in order to monitor evolution of viruses circulating in Vietnam The results of this study have implications for vaccine development and strategy and suggest a need for a continuous surveillance for this strain, especially after vaccine introduction Materials and methods 2.1 Samples We analyzed the fecal samples collected from children under years hospitalized for acute gastroenteritis These samples were collected in previous studies in 1998–1999, 2007–2008 and 2008–2009 seasons (Ngo et al., 2009; Nguyen et al., 2001) These samples have been stored at −20 ◦ C or −80 ◦ C The locations where the samples tested positive for rotavirus were collected and the time period are summarized in Table For each study site and each season, up to 10 samples were randomly selected among the G1P[8] positive samples for sequencing analysis of the VP7 gene All samples were delinked from patient identifiers and only the site and date of collection were maintained The rotavirus positive samples were genotyped as G1P[8] by nested RT-PCR following by sequencing of gene The samples were collected from the National Pediatric Hospital in Ha Noi (20 samples), Children’s Hospital No in Ho Chi Minh City (21 samples), Khanh Hoa General Hospital in Nha Trang city (19 samples) and Children’s Hospital in Hai Phong city (13 samples) during the years 1999–2009 in the rotavirus surveillance programs (Table 1) 191 RNA mini kit (Qiagen, GmbH, Germany), following manufacturer’s manual, aliquoted and stored at −80 ◦ C The reverse transcription reaction was performed using primer pair 9con1 and VP7R (Gouvea et al., 1990) The sequencing of the 897 bp amplicon was performed using an automated sequencing system (Genetic Analyzer 3130, Applied Biosystems, Inc., Foster City, CA) The comparison analysis was conducted on the G1 strains analyzed in the study and other G1 reference strains available in GenBank Ten samples representing the G1-VP7 sublineages in each region and period (1 sample/site/season) were selected for sequencing of 876 bp amplicons of the VP4 gene using con2 and con3 primers (Gentsch et al., 1992) The comparison analysis was conducted on the P[8] strains analyzed and other P[8] reference strains available in GenBank The sequence data and the phylogenetic analysis were carried out using BioEdit v7.0.5 Parsimony analysis was also conducted using MEGA version 5.0 to determine the evolutionary relationship (Tamura et al., 2007) among sequences studied The method was performed using neighbor-joining with a random option and 500 bootstrap repetitions The bootstrap value of ≥50 is presented Calculation of the accumulated mutation rate of VP7 gene in Vietnam over 11 years was made Sequence comparisons of the VP7 and VP4 genes investigated and those of G1 and P[8] reference strains available in GenBank were carried out The amino acid substitutions of the portion of the VP7 segment (amino acid positions 0–263) (nu 95–762) were counted and the annually accumulated mutation rate per site was calculated The VP4 and VP7 sequences of the Vietnamese strains analyzed in this study were submitted to GenBank with accession number JF690673–JF690745 and JN790709–JN790718 Reference VP7 sequences of G1 rotavirus strains and accession numbers used in this study are the following: strain Fin-408, accession no Z80303; Oh-64, U26387; Fin-431, Z80314; Cos70, U26370; Fin-111–1, Z80278; Au81, M64666; PA5-03, DQ377596; PA2-04, DQ377598; PA5, Q377573; PA164, DQ377588; ISO-4, AY098670; PA430, DQ377591; Thai-1604, DQ512981; PA378, DQ377589; Dhaka8, AY631049; Fin-429, Z80312; VN-281, DQ508167; Au007, AB081799; VN-355, DQ512968; Fin-101–1, Z80271; Thai-804, DQ512979; Fin-425-1, Z80309; Mvd9816, AF480293; G192B, AF043678; Mvd9810, AF480288; DC03, AF183850; 97′ S6, AF260945; CH631, AF183857; China-45, U26371; JP471, D16328; JPTE1, D17721; Wa, K02033; Egypt-8, U26374; HOU8697, U88717; JP-6916, EF079067; JP-7108, EF079068; JP-7014, EF079064; JP-7124, EF079069; JP-7206, EF079065; JP-7154, EF079070; Accession number of the VP7 sequence of USA/DS1/1976 (G2) is EF672581 Reference VP4 sequences of P[8] rotavirus strains and accession numbers used in this study are the following: RVA/Humanwt/KOR/CAU-202, EF059923; KOR/CAU-219, EU679394; THA/CU90P8, DQ235978; JPN/F45, U30716; MAL/OP354, AJ302148; CHN/WH-624, AY856444; MAL/MW670, AJ302146; IND/RMC437, AY603158; IND/Sc134 AJ293720; USA/Wa, M21843; CHN/WH-1194, AY85644; HUN/BP1829, AJ605319; JPN/Odelia, AB008296; THA/CU20, DQ235973; IND/ISO43, DQ355959 Accession number of the VP4 sequence of USA/DS1 (P[4]) is AB118025 Results 3.1 Analyses of VP7 genes from G1P[8] strains collected during 1998 and 2009 2.2 Sequencing of VP7 and VP4 regions Fecal samples were diluted in DEPC-treated water to make 20% suspension and the viral RNA was extracted using the Qiagen viral The VP7 genes of 73 G1P[8] rotavirus strains were sequenced and phylogenetic analysis was performed G1P[8] strains were obtained from each of the four cities (Ha Noi, Ho Chi Minh city, Hai 192 N.V Trang et al / Virus Research 165 (2012) 190–196 IB IA ID IC IE IIE IIA IID IIB IIC Fig Phylogenetic tree obtained from nucleotide sequence analyses on VP7 genes of G1 rotavirus isolated in Vietnam during 1998–1999 (in thin-line boxes), 2007–2008 (in thick-line boxes) and 2008–2009 (in dashed-line boxes) seasons Selected strains from different cities and rotavirus seasons within each G1-sublineage are depicted in this figure Reference strains were selected from GenBank (The GenBank accession numbers of reference strains and the Vietnamese strains identified in this study are indicated at the end of Section 2) Abbreviations of sites where the strains were isolated are as follows: HCMC, Ho Chi Minh city; HNI, Ha Noi; KH; Khanh Hoa and HP, Hai Phong N.V Trang et al / Virus Research 165 (2012) 190–196 193 Fig Phylogenetic tree obtained from nucleotide sequence analyses on VP4 genes of P[8] rotavirus isolated in Vietnam (in boxes) Reference strains were selected from GenBank (The GenBank accession numbers of reference strains and the Vietnamese strains identified in this study are indicated at the end of Section 2) Abbreviations of sites where the strains were isolated are the same as Fig Phong and Nha Trang) in the 1998–1999 and 2007–2008 seasons During the 1998–1999 (19 strains) and 2007–2008 (28 strains) seasons isolates were obtained from each of the four cities (Ha Noi, Ho Chi Minh city, Hai Phong and Nha Trang), while in 2008–2009 season isolates were obtained from all cities except Hai Phong (Table 1) All of the Vietnamese G1 strains analyzed in the study belonged to either lineage I or II Among the G1P[8] strains detected in the 1998–1999 season, lineages I (sublineages B, C, D and E) were identified in all cities and no lineage II strains were found (Fig 1) In 2008–2009 season, however, the majority of strains detected in all cities where samples were collected belonged to lineage IIC and only isolate of lineage I (D) was found (Fig 1) In 2007–2008 season in contrast, either lineage I (IB, ID, IE) or lineage II (IIC and IIE) G1 rotavirus were detected in all cities (Fig 1) Thus, it is likely that G1 strain circulating in Vietnam was changed from lineage I to II in the period between 1998 and 2009, particularly in the 2007–2008 season The lineage II (C) G1 rotaviruses detected in the 2008–2009 rotavirus season were highly homologous to each other in amino acid sequence irrespective of the site where the sample was collected (Fig 1) The VP4 genes of the selected 10 out of 73 G1P[8] strains (representing different G1-VP7 sublineages, different cities and rotavirus seasons) were analyzed and all grouped in F45-like cluster (Fig 2) Of note, the vaccine candidate strain Rotavin-M1 that was isolated in Nha Trang city in 2003, belongs to lineage I Rotarix (GSK) belongs to lineage II and the G1 strains of RotaTeq belong to lineage III, similar to Wa strain (Luan le et al., 2009; Matthijnssens et al., 2010b; Richardson et al., 1984) 3.2 Deduced amino acid differences between the VP7 proteins of lineage I and lineage II strains of G1 rotavirus The drift from lineage I to II was accompanied by amino acid substitutions at 13 positions including I29M, F37S, K49R, L55I, I57L, T65A, V66A, S68A, S94N, T108I, N123S, T217M, and I268V Applying the identification code system for different lineages proposed by Phan et al for amino acid position 29–75, lineage I can be described as IIYFVAALITSQGV and lineage II as MIYSVAAILAAQGI Conserved amino acid substitutions between lineages I and II, were also observed at other sites which were not part of Phan’s identification code including S94N, T108N, N123S, T217M and I268V In addition, one change each was identified in antigenic region A (at position 94) and C (position 217) of the protein, respectively (Fig 3) between lineage I and II strains In antigenic region B, the change S147N has been observed in several lineage I and II strains, but not in lineage III isolates (RotaTeq GI and Wa) Two amino acid differences 194 N.V Trang et al / Virus Research 165 (2012) 190–196 Fig Amino acid substitutions in the VP7 protein that are observed between lineages I and II Antigenic regions (A, B, C) are indicated Selected strains from different cities and rotavirus seasons within each sublineage are depicted in this figure Abbreviations of sites where the strains were isolated are the same as Fig The GenBank accession numbers of reference strains and the Vietnamese strains identified in this study are indicated at the end of Section between lineages I and II (V66A and I268V) that occurred during the time period 1998–2008 were maintained through the 2008–2009 season In contrast, only a single conserved amino acid substitution occurred in the VP7 protein of lineage II strains from 2007 to 2009, at position 41 (F41S) Some virus strains from Ha Noi, Hai Phong and Ho Chi Minh City have a change at position 91 (T91N) that has also been observed for strains in Japan and China Strains in Hai Phong from 2007 exhibit S at position 147 instead of N which was previously thought to be the signature for all G1 lineages except III Similarly, E but not D is common for all Vietnamese strains at position 97 The difference in amino acid sequence within lineage I strains from 1998 to 1999 and 2007 to 2008 seasons ranged from 0% to 3.6%, depending on study sites, whereas the difference in amino acid sequence of the protein between 2007–2008 and 2008–2009 seasons is smaller (0–0.8%) The amino acid difference between lineages I and II in different study sites ranged from 4.9% to 6.1% between 1998–1999 and 2008–2009 Based on the 13 amino acid changes over the 11 year period among the total 263 amino acid residues consisting antigenic sites of this protein available for analysis, we approximated the rate of accumulation of amino acid substitutions to be 0.9 × 10−3 /site/year Similarly, based on the 46 nucleotide changes over the 11 year period among the total 668 nucleotides of the gene under analysis, the rate of accumulation of nucleotide substitutions is estimated as 1.3 × 10−3 /site/year Discussion Rotavirus strain G1P[8] has been a globally dominant strain for more than 30 years and a number of studies have documented the great genetic variability of this genotype A study in Italy for strains collected over 19 years indicated the continuing appearance of rotavirus G1 variants (Arista et al., 2006) In the Italian study, Arista et al identified G1 lineages while Phan et al classified this genotype into 11 lineages based on the representative G1 strain sequences available worldwide (Arista et al., 2006; Phan et al., 2007) A study from Hungary also showed that G1 sublineages changed times over a 16 year period, suggesting that antigenic drifts occur periodically (Banyai et al., 2009) However, the study from Hungary also identified co-existence of lineages I and II in most seasons In the current study, we found that the G1P[8] strains circulating in Vietnam were diverse during the period 1998–1999 to 2007–2008, but were more conserved in 2008–2009 In 2008–2009, there was a drift from lineage I to II G1P[8] of the VP7 gene in Vietnam, while all the VP4 gene N.V Trang et al / Virus Research 165 (2012) 190–196 grouped in F45-like cluster The ability to observe such drifts in predominant strain lineages is possible only through long term surveillance, in this case over an 11 year time period In addition, because we conducted surveillance in different sites across the countries throughout this period, we were able to document that the drift in the predominant G1 lineage occurred throughout Vietnam Other studies conducted for shorter periods have not always observed distinct G1 lineages A study from Western India for time points from 1991 to 1994 and 2006 showed that lineage I was predominant at both time points (Arora et al., 2009) The G1 strain in the major cities of Australia in 1996 was extremely homogenous, with >99% nucleotide identity and >98.3% amino acid identity (Jayasinghe and Palombo, 1999) A study by Trinh et al showed that the G1 strain detected in Vietnam, Japan, China and Thailand during 2002–2005 fell into a single lineage (Trinh et al., 2007) Le et al found that the G1 detected in Korea during 2004–2006 belonged to lineage I (Le et al., 2010) Thus, the epidemiology of G1 strains is different depending on how long the sampling period is, the regions where the samples are collected It remains to be proven whether the genetic differences between lineages translate into antigenic differences In children vaccinated with a rotavirus vaccine who exhibited diarrhea due to Rotavirus, G1 strains were isolated which were different from the vaccine strains This observation suggests that the vaccines failed to provide protection against virus of different lineages (Matthijnssens et al., 2009) However, it remains to be seen whether all G1 vaccine failures will be due to strains in different G1 lineage from the vaccine strain Rotarix was developed from the 89–12 strain (isolated in 1989) belonging to lineage II the same lineage as most of the Vietnamese strains of 2009, but in a different lineage from those detected during 1998–1999 Lineage III of Wa and the RotaTeq G1 was not found in Vietnam during the years we surveyed (Matthijnssens et al., 2010b) However, among the G9P[8] lineages, lineage I is preferred over other lineages when including in the vaccine (Hoshino et al., 2004) Thus it is important to continue monitoring both genetic and antigenic difference between lineages of the same virus genotypes It is interesting to note that the strains became homogenous in 2008–2009 with all strains belonging to lineage IIC whereas in previous years, different sublineages of lineages I and II co-existed The reason for this strain convergence and switching is unknown In our study, the 14 amino acid identification code proposed by Phan et al for different VP7-G1 lineages is maintained However, we identified substitutions at other sites beyond this region (amino acid 29–75) and an additional substitution at amino acid 66 that could be used to differentiate between lineages I and II We also identified a change within lineage II (F41S) which has not previously been documented Strains detected in 2007 all have a T91N substitution as previously found only in China and Japan (Trinh et al., 2007) With the geographical proximity of Vietnam to China, and their active social and economical interactions prompted the virus movement across the countries Arora et al also documented several changes in this signature code for sublineage IB and IIB (Arora et al., 2009) Therefore it is suggested that the Phan’s identification code could be used as minimum requirement for distinguishing strains of different lineages and occasional updates using a larger numbers of strains from different time periods should be done Changes in nucleotide sequence are more significant when there is a corresponding amino acid substitution in the antigenic region For VP7, there are antigenic sites designated A (amino acid 87–101), B (amino acid 142–152), C (amino acid 208–221), D (amino acid 291) and F (amino acid 232–242) (Hoshino et al., 1994) We observed amino acid sequence differences between G1 lineages I and II in antigenic sites A and C, suggesting there might be 195 a corresponding change in antigenicity The signature amino acid N at position 147 (antigenic region B) for all lineages except lineage III does not apply to some of strains from Hai Phong Analysis using specific monoclonal antibodies to each of these sites could be one approach to study this hypothesis Even though information on the substitution rates for VP7 gene in Vietnam could not be found in previous studies, the rates of nucleotide and consequent deduced amino acid substitutions in VP7 region of G1 rotavirus are calculated as 0.9 × 10−3 /site/year and 1.3 × 10−3 /site/year, respectively, which are similar to those observed in a previous study (Matthijnssens et al., 2010a) In this study, we investigated changes in VP7 and VP4 genes However, it is necessary to monitor overall mutations dispersed across all 11 segments to identify global changes in the virus genome (Matthijnssens et al., 2008) These studies are valuable for assessment of vaccine and to see whether a novel strain will emerge and become predominant having evaded immunity provided by the vaccine Conflicts of interest None Acknowledgments The study was partly sponsored by the National Foundation for Science and Technology Development-Vietnam (PI Dang Duc Anh, project number 106.99.182.09) and Japan Initiative for Global Research Network on Infectious Diseases (J-GRID) for the sample collection and the sequencing analyses The portion of stool collection was funded by the World Health Organization (for the rotavirus surveillance program from 1998 to 2009 of N Van Man and L.T Luan) We sincerely thank Drs Anne-Lise Haenni (University of Paris), James Jones (Henry Jackson Foundation) and Jon R Gentsch (US-CDC) for critical reading of the manuscript References Arista, S., Giammanco, G.M., De Grazia, S., 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G1 vaccine failures will be due to strains in different G1 lineage from the vaccine strain Rotarix was developed from the 89–12 strain (isolated in 1989) belonging to lineage II the same lineage... However, among the G9P[8] lineages, lineage I is preferred over other lineages when including in the vaccine (Hoshino et al., 2004) Thus it is important to continue monitoring both genetic and antigenic... analysis of the VP7 gene of human rotavirus G1 isolated in Japan, China, Thailand, and Vietnam in the context of changing distribution of rotavirus G-types J Med Virol 79 (7), 1009–1016 Trinh, Q.D.,