Deep sequencing of norovirus genomes defines evolutionary patterns in an urban tropical setting

Journal of Virology

Volumn 88, Issue 19, 2014, Pages 11056-11069

  Cotten, Matthew ^a   Petrova, Velislava ^a   Phan, My V T ^b   Rabaa, Maia A ^b,c   Watson, Simon J ^a   Ong, Swee Hoe ^a   Kellam, Paul ^a,d   Baker, Stephen ^b,e,f  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b OXFORD UNIVERSITY CLINICAL RESEARCH UNIT   (Viet Nam)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 4; PROTEIN P22; PROTEIN P48; PROTEIN VP1; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CODON; DIARRHEA; EVOLUTIONARY RATE; GENE AMPLIFICATION; GENE SEQUENCE; GENETIC ALGORITHM; GENETIC CODE; HUMAN; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE; URBAN AREA; VIET NAM; VIRUS ASSEMBLY; VIRUS GENOME; CALICIVIRUS INFECTION; CHILD; CITY; CLASSIFICATION; EVOLUTION; GASTROENTERITIS; GENE EXPRESSION; GENETICS; HIGH THROUGHPUT SEQUENCING; INFANT; ISOLATION AND PURIFICATION; METHODOLOGY; PHYLOGENY; PRESCHOOL CHILD; VIROLOGY;

BIOLOGICAL EVOLUTION; CALICIVIRIDAE INFECTIONS; CHILD; CHILD, PRESCHOOL; CITIES; CODON; DIARRHEA; GASTROENTERITIS; GENE EXPRESSION; GENOME, VIRAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFANT; NOROVIRUS; PHYLOGENY; RNA, VIRAL; VIETNAM; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84906969109     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01333-14     Document Type: Article

References (59)

1. Thorne LG, Goodfellow IG. 2014. Norovirus gene expression and replication. J. Gen. Virol. 95:278-291. http://dx.doi.org/10.1099/vir.0 .059634-0.
2. McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y, Shortland A, Heeney J, Yarovinsky F, Simmonds P, Macdonald A, Goodfellow I. 2011. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog. 7(12):e1002413. http://dx.doi.org/10.1371/journal.ppat.1002413.
3. Sosnovtsev SV, Belliot G, Chang KO, Prikhodko VG, Thackray LB, Wobus CE, Karst SM, Virgin HW, Green KY. 2006. Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells. J. Virol. 80:7816-7831. http://dx.doi.org/10.1128/JVI .00532-06.
4. Wolf S, Williamson W, Hewitt J, Lin S, Rivera-Aban M, Ball A, Scholes P, Savill M, Greening GE. 2009. Molecular detection of norovirus in sheep and pigs in New Zealand farms. Vet. Microbiol. 133:184-189. http: //dx.doi.org/10.1016/j.vetmic.2008.06.019.
5. Wang QH, Han MG, Cheetham S, Souza M, Funk JA, Saif LJ. 2005. Porcine noroviruses related to human noroviruses. Emerg. Infect. Dis. 11:1874-1881. http://dx.doi.org/10.3201/eid1112.050485.
6. Wang QH, Chang KO, Han MG, Sreevatsan S, Saif LJ. 2006. Development of a new microwell hybridization assay and an internal control RNA for the detection of porcine noroviruses and sapoviruses by reverse transcription-PCR. J. Virol. Methods 132:135-145. http://dx.doi.org/10.1016 /j.jviromet.2005.10.003.
7. Sugieda M, Nakajima S. 2002. Viruses detected in the caecum contents of healthy pigs representing a new genetic cluster in genogroup II of the genus "Norwalk-like viruses." Virus Res. 87:165-172. http://dx.doi.org/10 .1016/S0168-1702(02)00107-7.
8. Oliver SL, Dastjerdi AM, Wong S, El-Attar L, Gallimore C, Brown DW, Green J, Bridger JC. 2003. Molecular characterization of bovine enteric caliciviruses: a distinct third genogroup of noroviruses (Norwalk-like viruses) unlikely to be of risk to humans. J. Virol. 77:2789-2798. http://dx .doi.org/10.1128/JVI.77.4.2789-2798.2003.
9. Martella V, Lorusso E, Decaro N, Elia G, Radogna A, D'Abramo M, Desario C, Cavalli A, Corrente M, Camero M, Germinario CA, Banyai K, Di Martino B, Marsilio F, Carmichael LE, Buonavoglia C. 2008. Detection and molecular characterization of a canine norovirus. Emerg. Infect. Dis. 14:1306-1308. http://dx.doi.org/10.3201/eid1408.080062.
10. Martella V, Campolo M, Lorusso E, Cavicchio P, Camero M, Bellacicco AL, Decaro N, Elia G, Greco G, Corrente M, Desario C, Arista S, Banyai K, Koopmans M, Buonavoglia C. 2007. Norovirus in captive lion cub (Panthera leo). Emerg. Infect. Dis. 13:1071-1073. http://dx.doi.org/10 .3201/eid1307.070268.
11. Liu BL, Lambden PR, Gunther H, Otto P, Elschner M, Clarke IN. 1999. Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. J. Virol. 73:819-825.
12. Hsu CC, Riley LK, Livingston RS. 2007. Molecular characterization of three novel murine noroviruses. Virus Genes 34:147-155. http://dx.doi .org/10.1007/s11262-006-0060-1.
13. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, Le Pendu J, Calderon RL. 2008. Norwalk virus: how infectious is it? J. Med. Virol. 80:1468-1476. http://dx.doi.org/10.1002/jmv.21237.
14. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Ramani S, Hill H, Ferreira J, Graham DY. 2014. Determination of the 50% human infectious dose for Norwalk virus. J. Infect. Dis. 209:1016-1022. http://dx.doi.org/10.1093/infdis/jit620.
15. Simmons K, Gambhir M, Leon J, Lopman B. 2013. Duration of immunity to norovirus gastroenteritis. Emerg. Infect. Dis. 19:1260-1267. http: //dx.doi.org/10.3201/eid1908.130472.
16. Debbink K, Lindesmith LC, Donaldson EF, Baric RS. 2012. Norovirus immunity and the great escape. PLoS Pathog. 8(10):e1002921. http://dx .doi.org/10.1371/journal.ppat.1002921.
17. Sukhrie FH, Teunis P, Vennema H, Copra C, Thijs Beersma MF, Bogerman J, Koopmans M. 2012. Nosocomial transmission of norovirus is mainly caused by symptomatic cases. Clin. Infect. Dis. 54:931-937. http: //dx.doi.org/10.1093/cid/cir971.
18. Siebenga JJ, Beersma MF, Vennema H, van Biezen P, Hartwig NJ, Koopmans M. 2008. High prevalence of prolonged norovirus shedding and illness among hospitalized patients: a model for in vivo molecular evolution. J. Infect. Dis. 198:994-1001. http://dx.doi.org/10.1086/591627.
19. Verhoef L, Williams KP, Kroneman A, Sobral B, van Pelt W, Koopmans M. 2012. Selection of a phylogenetically informative region of the norovirus genome for outbreak linkage. Virus Genes 44:8-18. http://dx.doi .org/10.1007/s11262-011-0673-x.
20. Sukhrie FH, Teunis P, Vennema H, Bogerman J, van Marm S, Beersma MF, Koopmans M. 2013. P2 domain profiles and shedding dynamics in prospectively monitored norovirus outbreaks. J. Clin. Virol. 56:286-292. http://dx.doi.org/10.1016/j.jcv.2012.12.006.
21. Bull RA, Eden JS, Luciani F, McElroy K, Rawlinson WD, White PA. 2012. Contribution of intra-and interhost dynamics to norovirus evolution. J. Virol. 86:3219-3229. http://dx.doi.org/10.1128/JVI.06712-11.
22. Kundu S, Lockwood J, Depledge DP, Chaudhry Y, Aston A, Rao K, Hartley JC, Goodfellow I, Breuer J. 2013. Next-generation whole genome sequencing identifies the direction of norovirus transmission in linked patients. Clin. Infect. Dis. 57:407-414. http://dx.doi.org/10.1093 /cid/cit287.
23. Lindesmith L, Moe C, Lependu J, Frelinger JA, Treanor J, Baric RS. 2005. Cellular and humoral immunity following Snow Mountain virus challenge. J. Virol. 79:2900-2909. http://dx.doi.org/10.1128/JVI.79.5 .2900-2909.2005.
24. Cannon JL, Lindesmith LC, Donaldson EF, Saxe L, Baric RS, Vinje J. 2009. Herd immunity to GII.4 noroviruses is supported by outbreak patient sera. J. Virol. 83:5363-5374. http://dx.doi.org/10.1128/JVI.02518-08.
25. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. 2008. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol. Rev. 225:190-211. http://dx.doi.org/10.1111/j .1600-065X.2008.00680.x.
26. Lindesmith LC, Beltramello M, Donaldson EF, Corti D, Swanstrom J, Debbink K, Lanzavecchia A, Baric RS. 2012. Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog. 8(5): e1002705. http://dx.doi.org/10.1371/journal.ppat.1002705.
27. LoBue AD, Lindesmith L, Yount B, Harrington PR, Thompson JM, Johnston RE, Moe CL, Baric RS. 2006. Multivalent norovirus vaccines induce strong mucosal and systemic blocking antibodies against multiple strains. Vaccine 24:5220-5234. http://dx.doi.org/10.1016/j.vaccine.2006 .03.080.
28. Lindesmith LC, Donaldson E, Leon J, Moe CL, Frelinger JA, Johnston RE, Weber DJ, Baric RS. 2010. Heterotypic humoral and cellular immune responses following Norwalk virus infection. J. Virol. 84:1800-1815. http://dx.doi.org/10.1128/JVI.02179-09.
29. Reeck A, Kavanagh O, Estes MK, Opekun AR, Gilger MA, Graham DY, Atmar RL. 2010. Serological correlate of protection against norovirusinduced gastroenteritis. J. Infect. Dis. 202:1212-1218. http://dx.doi.org /10.1086/656364.
30. My PV, Thompson C, Phuc HL, Tuyet PT, Vinh H, Hoang NV, Minh PV, Vinh NT, Thuy CT, Nga TT, Hau NT, Campbell J, Chinh NT, Thuong TC, Tuan HM, Farrar J, Baker S. 2013. Endemic norovirus infections in children, Ho Chi Minh City, Vietnam, 2009-2010. Emerg. Infect. Dis. 19:977-980. http://dx.doi.org/10.3201/eid1906.111862.
31. Tra My PV, Lam HM, Thompson CN, Phuc HL, Tuyet PT, Vinh H, Hoang NV, Minh P, Vinh NT, Thuy CT, Nga TT, Hau NT, Chinh NT, Thuong TC, Tuan HM, Campbell JI, Clements AC, Farrar J, Boni MF, Baker S. 2013. The dynamics of GII.4 norovirus in Ho Chi Minh City, Vietnam. Infect. Genet. Evol. 18:335-343. http://dx.doi.org/10.1016/j .meegid.2013.04.014.
32. Cotten M, Lam TT, Watson SJ, Palser AL, Petrova V, Grant P, Pybus OG, Rambaut A, Guan Y, Pillay D, Kellam P, Nastouli E. 2013. Full-genome deep sequencing and phylogenetic analysis of novel human betacoronavirus. Emerg. Infect. Dis. 19:736-742. http://dx.doi.org/10 .3201/eid1905.130057.
33. Quail MA, Otto TD, Gu Y, Harris SR, Skelly TF, McQuillan JA, Swerdlow HP, Oyola SO. 2012. Optimal enzymes for amplifying sequencing libraries. Nat. Methods 9:10-11. http://dx.doi.org/10.1038 /nchembio.1143.
34. Quail MA, Kozarewa I, Smith F, Scally A, Stephens PJ, Durbin R, Swerdlow H, Turner DJ. 2008. A large genome center's improvements to the Illumina sequencing system. Nat. Methods 5:1005-1010. http://dx.doi .org/10.1038/nmeth.1270.
35. Watson SJ, Welkers MR, Depledge DP, Coulter E, Breuer JM, de Jong MD, Kellam P. 2013. Viral population analysis and minority-variant detection using short read next-generation sequencing. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20120205. http://dx.doi.org/10.1098/rstb.2012 .0205.
36. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to singlecell sequencing. J. Comput. Biol. 19:455-477. http://dx.doi.org/10.1089 /cmb.2012.0021.
37. Martin D, Rybicki E. 2000. RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562-563. http://dx.doi.org/10.1093 /bioinformatics/16.6.562.
38. Dubot-Pe`re´s A, Vongphrachanh P, Denny J, Phetsouvanh R, Linthavong S, Sengkeopraseuth B, Khasing A, Xaythideth V, Moore CE, Vongsouvath M, Castonguay-Vanier J, Sibounheuang B, Taojaikong T, Chanthongthip A, de Lamballerie X, Newton PN. 2013. An epidemic of dengue-1 in a remote village in rural Laos. PLoS Negl. Trop. Dis. 7(8): e2360. http://dx.doi.org/10.1371/journal.pntd.0002360.
39. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
40. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772. http: //dx.doi.org/10.1038/nmeth.2109.
41. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29:1969-1973. http://dx.doi.org/10.1093/molbev/mss075.
42. Minin VN, Bloomquist EW, Suchard MA. 2008. Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol. Biol. Evol. 25:1459-1471. http://dx.doi.org/10.1093 /molbev/msn090.
43. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. 2012. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8(7):e1002764. http://dx.doi.org/10.1371/journal .pgen.1002764.
44. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K. 2013. FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol. Biol. Evol. 30:1196-1205. http: //dx.doi.org/10.1093/molbev/mst030.
45. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. 2010. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455-2457. http://dx.doi.org/10.1093/bioinformatics /btq429.
46. Pond SLK, Frost SD, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679. http://dx.doi.org/10.1093 /bioinformatics/bti079.
47. Kroneman A, Vennema H, Deforche K, van der Avoort H, Peñaranda S, Oberste MS, Vinje´ J, Koopmans M. 2011. An automated genotyping tool for enteroviruses and noroviruses. J. Clin. Virol. 51:121-125. http://dx.doi .org/10.1016/j.jcv.2011.03.006.
48. Chan MC, Lee N, Ho WS, Law CO, Lau TC, Tsui SK, Sung JJ. 2012. Covariation of major and minor viral capsid proteins in norovirus genogroup II genotype 4 strains. J. Virol. 86:1227-1232. http://dx.doi.org/10 .1128/JVI.00228-11.
49. Siebenga JJ, Lemey P, Kosakovsky Pond SL, Rambaut A, Vennema H, Koopmans M. 2010. Phylodynamic reconstruction reveals norovirus GII.4 epidemic expansions and their molecular determinants. PLoS Pathog. 6(5):e1000884. http://dx.doi.org/10.1371/journal.ppat.1000884.
50. Bok K, Abente EJ, Realpe-Quintero M, Mitra T, Sosnovtsev SV, Kapikian AZ, Green KY. 2009. Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J. Virol. 83:11890-11901. http://dx.doi.org/10 .1128/JVI.00864-09.
51. Boon D, Mahar JE, Abente EJ, Kirkwood CD, Purcell RH, Kapikian AZ, Green KY, Bok K. 2011. Comparative evolution of GII.3 and GII.4 norovirus over a 31-year period. J. Virol. 85:8656-8666. http://dx.doi.org/10 .1128/JVI.00472-11.
52. Vongpunsawad S, Venkataram Prasad BV, Estes MK. 2013. Norwalk virus minor capsid protein VP2 associates within the VP1 shell domain. J. Virol. 87:4818-4825. http://dx.doi.org/10.1128/JVI.03508-12.
53. Zhu S, Regev D, Watanabe M, Hickman D, Moussatche N, Jesus DM, Kahan SM, Napthine S, Brierley I, Hunter RN, III, Devabhaktuni D, Jones MK, Karst SM. 2013. Identification of immune and viral correlates of norovirus protective immunity through comparative study of intracluster norovirus strains. PLoS Pathog. 9(9):e1003592. http://dx.doi.org /10.1371/journal.ppat.1003592.
54. de Rougemont A, Ruvoen-Clouet N, Simon B, Estienney M, Elie-Caille C, Aho S, Pothier P, Le Pendu J, Boireau W, Belliot G. 2011. Qualitative and quantitative analysis of the binding of GII.4 norovirus variants onto human blood group antigens. J. Virol. 85:4057-4070. http://dx.doi.org/10 .1128/JVI.02077-10.
55. Debbink K, Donaldson EF, Lindesmith LC, Baric RS. 2012. Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J. Virol. 86:1214-1226. http: //dx.doi.org/10.1128/JVI.06189-11.
56. Sharp TM, Crawford SE, Ajami NJ, Neill FH, Atmar RL, Katayama K, Utama B, Estes MK. 2012. Secretory pathway antagonism by calicivirus homologues of Norwalk virus nonstructural protein p22 is restricted to noroviruses. Virol. J. 9:181. http://dx.doi.org/10.1186/1743-422X-9-181.
57. Sharp TM, Guix S, Katayama K, Crawford SE, Estes MK. 2010. Inhibition of cellular protein secretion by Norwalk virus nonstructural protein p22 requires a mimic of an endoplasmic reticulum export signal. PLoS One 5(10):e13130. http://dx.doi.org/10.1371/journal.pone.0013130.
58. Ettayebi K, Hardy ME. 2003. Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein. J. Virol. 77:11790-11797. http://dx.doi.org/10.1128/JVI.77.21.11790-11797.2003.
59. Breslauer KJ, Frank R, Blocker H, Marky LA. 1986. Predicting DNA duplex stability from the base sequence. Proc. Natl. Acad. Sci. U. S. A. 83:3746-3750. http://dx.doi.org/10.1073/pnas.83.11.3746.