Whole genome analyses of African G2, G8, G9, and G12 rotavirus strains using sequence-independent amplification and 454® pyrosequencing

Journal of Medical Virology

Volumn 83, Issue 11, 2011, Pages 2018-2042

  Jere, Khuzwayo C ^a   Mlera, Luwanika ^a   O'Neill, Hester G ^a   Potgieter, A Christiaan ^b   Page, Nicola A ^c   Seheri, Mapaseka L ^d   van Dijk, Alberdina A ^a  

^a NORTH WEST UNIVERSITY   (South Africa)

^b Deltamune (Pty) Ltd   (South Africa)

^c NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^d SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

Author keywords

454 pyrosequencing; Emerging strains; Genogroup; Rotavirus

Indexed keywords

COMPLEMENTARY DNA;

AFRICA; ARTICLE; DNA SYNTHESIS; G12 ROTAVIRUS; G2 ROTAVIRUS; G8 ROTAVIRUS; G9 ROTAVIRUS; GENE AMPLIFICATION; GENOME ANALYSIS; GENOTYPE; INTERNET; NONHUMAN; PHYLOGENY; PYROSEQUENCING; ROTAVIRUS; VIRUS STRAIN;

AFRICA; DNA PRIMERS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, VIRAL; GENOTYPE; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; REASSORTANT VIRUSES; RECOMBINATION, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; ROTAVIRUS; ROTAVIRUS INFECTIONS; SEQUENCE ANALYSIS, DNA;

ARTIODACTYLA; BOVINAE; HUMAN ROTAVIRUS A; ROTAVIRUS;

EID: 80052750696     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.22207     Document Type: Article

References (54)

1. Ball JM, Tian P, Zeng CQ, Morris AP, Estes MK. 1996. Age-dependend diarrhea induced by a rotaviral non-structural rotavirus receptor glycoprotein. Science 272: 101-104.
2. Bányai K, Mijatovic-Rustempasic S, Hull JJ, Esona MD, Freeman MM, Frace AM, Bowen MD, Gentsch JR. 2011. Sequencing and phylogenetic analysis of the coding region of six common rotavirus strains: Evidence for intragenogroup reassortment among co-circulating G1P[8] and G2P[4] strains from the United States. J Med Virol 83: 532-539.
3. Bruenn JA. 1991. Relationships among the positive strand and double-strand RNA viruses as viewed through their RNA-dependent RNA polymerases. Nucl Acids Res 19: 217-226.
4. Ciarlet M, Hidalgo M, Gorziglia M, Liprandi F. 1994. Characterization of neutralization epitopes on the VP7 surface protein of serotype G11 porcine rotaviruses. J Gen Virol 75: 1867-1873.
5. Ciarlet M, Hoshino Y, Liprandi F. 1997. Single point mutations may affect the serotype reactivity of serotype G11 porcine rotavirus strains: A widening spectrum? J Virol 71: 8213-8220.
6. Ciarlet M, Hyser J, Estes MK. 2002. Sequence analysis of the VP4, VP6, VP7, and NSP4 gene products of the bovine rotavirus WC3. Virus Genes 24: 107-118.
7. Crawford S, Mukherjee S, Estes MK, Lawton J, Shaw A, Ramig RF, Prasad BV. 2001. Trypsin cleavage stabilizes the rotavirus VP4 spike. J Virol 75: 6052-6061.
8. Cunliffe NA, Gondwe JS, Broadhead RL, Molyneux ME, Woods PA, Bresee JS, Glass RI, Gentsch JR, Hart CA. 1999. Rotavirus G and P types in children with acute diarrhea in Blantyre, Malawi, from 1997 to 1998: Predominance of novel P[6]G8 strains. J Med Virol 57: 308-312.
9. Cunliffe NA, Gentsch JR, Kirkwood CD, Gondwe JS, Dove W, Nakagomi O, Nakagomi T, Hoshino Y, Bresee JS, Glass RI, Molyneux ME, Hart CA. 2000. Molecular and serologic characterization of novel serotype G8 human rotavirus strains detected in Blantyre, Malawi. Virology 274: 309-3020.
10. Das BK, Gentsch JR, Ciricello HG, Woods PA, Gupta A, Ramachandran M, Kumar R, Bhan MK, Glass RI. 1994. Characterization of rotavirus strains from newborns in New Delhi, India. J Clin Microbiol 32: 1820-1822.
11. De Grazia S, Giammanco GM, Potgieter CA, Matthijnssens J, Banyai K, Platia MA, Colomba C, Martella V. 2010. Unusual assortment of segments in 2 rare human rotavirus genomes. Emerg Infect Dis 16: 859-862.
12. Dyall-Smith ML, Lazdins I, Tregear GW, Holmes IH. 1986. Location of the major antigenic sites involved in rotavirus serotype specific neutralization. Proc Natl Acad Sci USA 83: 3465-3468.
13. Esona MD, Geyer A, Page N, Trabelsi A, Fodha I, Aminu M, Agbaya VA, Tsion B, Kerin TK, Armah GE, Steele AD, Glass RI, Gentsch JR. 2009. Genomic characterization of human rotavirus G8 strains from the African rotavirus network: Relationship to animal rotaviruses. J Med Virol 81: 937-951.
14. Estes MK, Kapikian AZ. 2007. Rotaviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, editors. Fields virology. Philadelphia: Lippincott Williams & Wilkins/Wolters Kluwer, pp 1917-1974.
15. Gentsch JR, Laird AR, Belfelt B, Bielfelt B, Griffin DD, Banyai K, Ramachandran M, Jain V, Cunliffe NA, Nakagomi O, Kirkwood CD, Fischer TK, Parashar UD, Bresee JS, Jiang B, Glass RI. 2005. Serotype diversity and reassortment between human and animal rotavirus strains: Implication for rotavirus vaccine programs. J Infect Dis 192: S146-S159.
16. Gorziglia M, Green K, Hoshino Y, Nishikawa K, Taniguchi K, Jones R, Kapikian AZ, Chonock RM. 1988. Sequence of the fourth gene of human rotaviruses recovered from asymptomatic and symptomatic infections. J Virol 62: 2978-2984.
17. Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, Fang ZY. 1990. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28: 276-282.
18. Gray J, Vesikari T, Van Damme P, Giaquinto C, Mrukowicz J, Guarino A, Dagan R, Szajewska H, Usonis V. 2008. Rotavirus. J Pediatr Gastroenterol Nutr 46: S24-S31.
19. Greenberg HB, Kalica AR, Wyatt RG, Jones RW, Kapikian AZ, Chanock RM. 1981. Rescue of noncultivatable human rotavirus by gene reassortment during mixed infection with its mutants of a cultivatable bovine rotavirus. Proc Natl Acad Sci USA 78: 420-424.
20. Gurgel RQ, Cuevas LE, Vieira SC, Barros VC, Fontes PB, Salustino EF, Nakagomi O, Nakagomi T, Dove W, Cunliffe N, Hart CA. 2007. Predominance of rotavirus P[4]G2 in a vaccinated population, Brazil. Emerg Infect Dis 13: 1571-1573.
21. Hall TA. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
22. Heiman EM, McDonald SM, Barro M, Taraporewala ZF, Bar-Magen T, Patton JT. 2008. Group A human rotavirus genomics: Evidence that gene constellations are influenced by viral protein interactions. J Virol 82: 11106-11116.
23. Hua J, Mansell E, Patton JT. 1993. Comparative analysis of the rotavirus NS53 gene: Conservation of basic and cysteine-rich regions in the protein and possible stemloop structures in the RNA. Virology 196: 372-378.
24. Ito H, Sugiyama M, Masubuchi K, Mori Y, Minamoto N. 2001. Complete nucleotide sequence of a group A avian rotavirus genome and a comparison with its counterparts of mammalian rotaviruses. Virus Res 75: 123-138.
25. Iturriza-Gómara M, Kang G, Gray J. 2004. Rotavirus genotyping: Keeping up with an evolving population of human rotaviruses. J Clin Microbiol 31: 259-265.
26. Kirkwood CD, Boniface K, Barnes GL, Bishop RF. 2011. Distribution of rotavirus genotypes after introduction of rotavirus vaccines, Rotarix® and RotaTeq®, into the National Immunization Program of Australia. Pediatr Infect Dis J 30: S48-S53.
27. Kumar A, Charpilienne A, Cohen J. 1989. Nucleotide sequence of the gene encoding for the RNA binding protein (VP2) of RF bovine rotavirus. Nucl Acids Res 17: 2126.
28. Le VP, Kim JY, Cho SL, Nam SW, Lim I, Lee HJ, Kim K, Chung SI, Song W, Lee KM, Rhee MS, Lee JS, Kim W. 2008. Detection of unusual rotavirus genotypes G8P[8] and G12P[6] in South Korea. J Med Virol 80: 175-182.
29. Maes P, Matthijnssens J, Rahman M, Van Ranst M. 2009. RotaC: A web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol 9: 238.
30. Martella V, Bányai K, Matthijnssens J, Buonavoglia C, Ciarlet M. 2010. Zoonotic aspects of rotaviruses. Vet Microbiol 140: 246-255.
31. Matthijnssens J, Rahman M, Yang X, Delbeke T, Arijs I, Kabue JP, Muyembe JJ, Van Ranst M. 2006. G8 rotavirus strains isolated in the Democratic Republic of Congo belong to the DS-1-like genogroup. J Clin Microbiol 44: 1801-1809.
32. Matthijnssens J, Rahman M, Van Ranst M. 2008a. Two out of the 11 genes of an unusual human G6P[6] rotavirus isolate are of bovine origin. J Gen Virol 89: 2630-2635.
33. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gómara M, Maes P, Patton JT, Rahman M, Van Ranst M. 2008b. Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82: 3204-3219.
34. Matthijnssens J, Potgieter CA, Ciarlet M, Parreño V, Martella V, Bányai K, Garaicoechea L, Palombo EA, Novo L, Zeller M, Arista S, Gerna G, Rahman M, Van Ranst M. 2009. Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla? J Virol 83: 2917-2929.
35. Matthijnssens J, Heylen E, Zeller M, Rahman M, Lemey P, Van Ranst M. 2010. Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol Biol Evol 27: 2431-2436.
36. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K, Brister JR, Buesa J, Esona MD, Estes MK, Gentsch JR, Iturriza-Gómara M, Johne R, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Parreño V, Rahman M, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Patton JT, Desselberger U, Van Ranst M. 2011. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol [Epub ahead of print 20 May].
37. Mattion NM, Cohen J, Aponte C, Estes MK. 1992. Characterization of an oligomerization domain and RNA binding properties on rotavirus nonstructural protein NS34. Virology 190: 68-83.
38. Mijatovic-Rustempasic S, Bányai K, Esona MD, Foytich K, Bowen MD, Gentsch JR. 2011. Genome sequence based molecular epidemiology of unusual US Rotavirus A G9 strains isolated from Omaha, USA between 1997 and 2000. Infect Genet Evol 11: 522-527.
39. Mitchell DB, Both GW. 1990. Completion of the genomic sequence of the simian rotavirus SA11: Nucleotide sequences of segments 1, 2, and 3. Virology 177: 324-331.
40. Mukherjee A, Dutta D, Ghosh S, Bagchi P, Chattopadhyay S, Nagashima S, Kobayashi N, Dutta P, Krishnan T, Naik TN, Chawla-Sarkar M. 2009. Full genomic analysis of a human group A rotavirus G9P[6] strain from Eastern India provides evidence for porcine-to-human interspecies transmission. Arch Virol 154: 733-746.
41. Mwenda JM, Ntoto KM, Abebe A, Enweronu-Laryea C, Amina I, Mchomvu J, Kisakye A, Mpabalwani EM, Pazvakavambwa I, Armah GE, Seheri LM, Kiulia NM, Page N, Widdowson MA, Steele AD. 2010. Burden and epidemiology of rotavirus diarrhea in selected African countries: Preliminary results from the African Rotavirus Surveillance Network. J Infect Dis 202: S5-S11.
42. Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, Steele D, Birmingham M, Glass RI. 2009. Global mortality associated with rotavirus disease among children in 2004. J Infect Dis 200: S9-S15.
43. Patton JT, Salter-Cid L, Kalbach A, Mansell EA, Kattoura M. 1993. Nucleotide and amino acid sequence analysis of the rotavirus nonstructural RNA-binding protein NS35. Virology 192: 438-446.
44. Potgieter AC, Page NA, Liebenberg J, Wright IM, Landt O, van Dijk AA. 2009. Improved strategies for sequence-independent amplification and sequencing of viral double-stranded RNA genomes. J Gen Virol 90: 1423-1432.
45. Rahman M, Matthijnssens J, Yang X, Delbeke T, Arijs I, Taniguchi K, Iturriza-Gómara M, Iftekharuddin N, Azim T, Van Ranst M. 2007. Evolutionary history and global spread of the emerging G12 human rotaviruses. J Virol 81: 2382-2390.
46. Ruiz-Palacios GM, Perez-Schael I, Velazquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, Cervantes Y, Linhares AC, López P, Macías-Parra M, Ortega-Barría E, Richardson V, Rivera-Medina DM, Rivera L, Salinas B, Pavía-Ruz N, Salmerón J, Rüttimann R, Tinoco JC, Rubio P, Nuñez E, Guerrero ML, Yarzábal JP, Damaso S, Tornieporth N, Sáez-Llorens X, Vergara RF, Vesikari T, Bouckenooghe A, Clemens R, De Vos B, O'Ryan M, Human Rotavirus Vaccine Study Group. 2006. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Eng J Med 354: 11-22.
47. Sanchez-Padilla E, Grais RF, Guerin PJ, Steele AD, Burny ME, Lacquer FJ. 2009. Burden of disease and circulating serotypes of rotavirus infection in sub-Saharan Africa: Systematic review and meta-analysis. Lancet Infect Dis 9: 567-576.
48. Santos N, Hoshino H. 2005. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective vaccine. Rev Med Virol 15: 29-56.
49. Stirzaker SC, Whitfeld PL, Christie DL, Bellamy AR, Both GW. 1987. Processing of rotavirus glycoprotein VP7: Implications for the retention of the protein in the endoplasmic reticulum. J Cell Biol 105: 2897-2903.
50. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
51. Tang B, Gilbert JM, Matsui SM, Greenberg HB. 1997. Comparison of the rotavirus gene 6 from different species by sequence analysis and localization of subgroup-specific epitopes using site-directed mutagenesis. Virology 237: 89-96.
52. Todd S, Page NA, Steele AD, Peenze I, Cunliffe NA. 2010. Rotavirus strain types circulating in Africa: Review of studies published during 1997-2006. J Infect Dis 202: S34-S42.
53. Tsugawa T, Hoshino Y. 2008. Whole genome sequence and phylogenetic analyses reveal human rotavirus G3P[3] strains Ro1845 and HCR3A are examples of direct virion transmission of canine/feline rotaviruses to humans. Virology 380: 344-353.
54. World Heath Organisation (WHO). 2008. Weekly epidemiological record. Wkly Epidemiol Records, no. 32 82: 285-296.