G8 rotaviruses with conserved genotype constellations detected in Malawi over 10 years (1997-2007) display frequent gene reassortment among strains co-circulating in humans

Journal of General Virology

Volumn 94, Issue PART 6, 2013, Pages 1273-1295

  Nakagomi, Toyoko ^a,b   Doan, Yen Hai ^a   Dove, Winifred ^b   Ngwira, Bagrey ^c   Iturriza Gómara, Miren ^b   Nakagomi, Osamu ^a,b   Cunliffe, Nigel A ^b  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF MALAWI   (Malawi)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CULTURE; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC REASSORTMENT; GENOTYPE; MALAWI; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; ROTAVIRUS; VIRAL GASTROENTERITIS; VIRUS GENOME; VIRUS STRAIN;

EID: 84877989705     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.050625-0     Document Type: Article

References (50)

1. Adah, M. I., Nagashima, S., Wakuda, M. & Taniguchi, K. (2003). Close relationship between G8-serotype bovine and human rotaviruses isolated in Nigeria. J Clin Microbiol 41, 3945-3950.
2. Alkan, F., Ozkul, A., Oguzoglu, T. C., Timurkan, M. O., Caliskan, E., Martella, V. & Burgu, I. (2010). Distribution of G (VP7) and P (VP4) genotypes of group A bovine rotaviruses from Turkish calves with diarrhea, 1997-2008. Vet Microbiol 141, 231-237.
3. Bányai, K., Martella, V., Molnár, P., Mihály, I., Van Ranst, M. & Matthijnssens, J. (2009). Genetic heterogeneity in human G6P[14] rotavirus strains detected in Hungary suggests independent zoonotic origin. J Infect 59, 213-215.
4. Bányai, K., Papp, H., Dandár, E., Molnár, P., Mihály, I., Van Ranst, M., Martella, V. & Matthijnssens, J. (2010). Whole genome sequencing and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain. Infect Genet Evol 10, 1140-1144.
5. Bányai, K., Mijatovic-Rustempasic, S., Hull, J. J., Esona, M. D., Freeman, M. M., Frace, A. M., Bowen, M. D. & Gentsch, J. R. (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.
6. Bányai, K., László, B., Duque, J., Steele, A. D., Nelson, E. A., Gentsch, J. R. & Parashar, U. D. (2012). Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 30 (Suppl 1), A122-A130.
7. Chen, Y., Wen, Y., Liu, X., Xiong, X., Cao, Z., Zhao, Q., Yu, Y., Yin, X., Li, C. & Fan, Y. (2008). Full genomic analysis of human rotavirus strain TB-Chen isolated in China. Virology 375, 361-373.
8. Cunliffe, N. A., Gondwe, J. S., Broadhead, R. L., Molyneux, M. E., Woods, P. A., Bresee, J. S., Glass, R. I., Gentsch, J. R. & Hart, C. A. (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, N. A., Gentsch, J. R., Kirkwood, C. D., Gondwe, J. S., Dove, W., Nakagomi, O., Nakagomi, T., Hoshino, Y., Bresee, J. S. & other authors (2000). Molecular and serologic characterization of novel serotype G8 human rotavirus strains detected in Blantyre, Malawi. Virology 274, 309-320.
10. Cunliffe, N. A., Gondwe, J. S., Graham, S. M., Thindwa, B. D., Dove, W., Broadhead, R. L., Molyneux, M. E. & Hart, C. A. (2001). Rotavirus strain diversity in Blantyre, Malawi, from 1997 to 1999. J Clin Microbiol 39, 836-843.
11. Cunliffe, N. A., Ngwira, B. M., Dove, W., Thindwa, B. D., Turner, A. M., Broadhead, R. L., Molyneux, M. E. & Hart, C. A. (2010). Epidemiology of rotavirus infection in children in Blantyre, Malawi, 1997-2007. J Infect Dis 202 (Suppl), S168-S174.
12. De Grazia, S., Giammanco, G. M., Potgieter, C. A., Matthijnssens, J., Banyai, K., Platia, M. A., Colomba, C. & Martella, V. (2010). Unusual assortment of segments in 2 rare human rotavirus genomes. Emerg Infect Dis 16, 859-862.
13. Desselberger, U. & Huppertz, H. I. (2011). Immune responses to rotavirus infection and vaccination and associated correlates of protection. J Infect Dis 203, 188-195.
14. Doan, Y. H., Nakagomi, T. & Nakagomi, O. (2012). Repeated circulation over 6 years of intergenogroup mono-reassortant G2P[4] rotavirus strains with genotype N1 of the NSP2 gene. Infect Genet Evol 12, 1202-1212.
15. Doan, Y. H., Nakagomi, T., Aboudy, Y., Silberstein, I., Behar-Novat, E., Nakagomi, O. & Shulman, L. M. (2013). Identification by fullgenome analysis of a bovine rotavirus transmitted directly to and causing diarrhea in a human child. J Clin Microbiol 51, 182-189.
16. Franco, M. A., Angel, J. & Greenberg, H. B. (2006). Immunity and correlates of protection for rotavirus vaccines. Vaccine 24, 2718-2731.
17. Ghosh, S., Alam, M. M., Ahmed, M. U., Talukdar, R. I., Paul, S. K. & Kobayashi, N. (2010). Complete genome constellation of a caprine group A rotavirus strain reveals common evolution with ruminant and human rotavirus strains. J Gen Virol 91, 2367-2373.
18. Ghosh, S., Paul, S. K., Hossain, M. A., Alam, M. M., Ahmed, M. U. & Kobayashi, N. (2011a). Full genomic analyses of two human G2P[4] rotavirus strains detected in 2005: identification of a caprine-like VP3 gene. J Gen Virol 92, 1222-1227.
19. Ghosh, S., Adachi, N., Gatheru, Z., Nyangao, J., Yamamoto, D., Ishino, M., Urushibara, N. & Kobayashi, N. (2011b). Whole-genome analysis reveals the complex evolutionary dynamics of Kenyan G2P[4] human rotavirus strains. J Gen Virol 92, 2201-2208.
20. Ghosh, S., Gatheru, Z., Nyangao, J., Adachi, N., Urushibara, N. & Kobayashi, N. (2011c). Full genomic analysis of a G8P[1] rotavirus strain isolated from an asymptomatic infant in Kenya provides evidence for an artiodactyl-to-human interspecies transmission event. J Med Virol 83, 367-376.
21. Heiman, E. M., McDonald, S. M., Barro, M., Taraporewala, Z. F., Bar-Magen, T. & Patton, J. T. (2008). Group A human rotavirus genomics: evidence that gene constellations are influenced by viral protein interactions. J Virol 82, 11106-11116.
22. Iturriza-Gómara, M., Isherwood, B., Desselberger, U. & Gray, J. (2001). Reassortment in vivo: driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999. J Virol 75, 3696-3705.
23. Jere, K. C., Mlera, L., O'Neill, H. G., Potgieter, A. C., Page, N. A., Seheri, M. L. & van Dijk, A. A. (2011). Whole genome analyses of African G2, G8, G9, and G12 rotavirus strains using sequenceindependent amplification and 4541pyrosequencing. J Med Virol 83, 2018-2042.
24. Jere, K. C., Mlera, L., O'Neill, H. G., Peenze, I. & van Dijk, A. A. (2012). Whole genome sequence analyses of three African bovine rotaviruses reveal that they emerged through multiple reassortment events between rotaviruses from different mammalian species. Vet Microbiol 159, 245-250.
25. Kutsuzawa, T., Konno, T., Suzuki, H., Kapikian, A. Z., Ebina, T. & Ishida, N. (1982). Isolation of human rotavirus subgroups 1 and 2 in cell culture. J Clin Microbiol 16, 727-730.
26. 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.
27. Matsuno, S., Hasegawa, A., Mukoyama, A. & Inouye, S. (1985). A candidate for a new serotype of human rotavirus. J Virol 54, 623-624.
28. Matthijnssens, J., Rahman, M., Yang, X., Delbeke, T., Arijs, I., Kabue, J. P., Muyembe, J. J. & 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.
29. Matthijnssens, J., Ciarlet, M., Heiman, E., Arijs, I., Delbeke, T., McDonald, S. M., Palombo, E. A., Iturriza-Gómara, M., Maes, P. & other authors (2008a). 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.
30. Matthijnssens, J., Rahman, M. & Van Ranst, M. (2008b). Two out of the 11 genes of an unusual human G6P[6] rotavirus isolate are of bovine origin. J Gen Virol 89, 2630-2635.
31. Matthijnssens, J., Potgieter, C. A., Ciarlet, M., Parreño, V., Martella, V., Bányai, K., Garaicoechea, L., Palombo, E. A., Novo, L. & other authors (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.
32. Matthijnssens, J., Taraporewala, Z. F., Yang, H., Rao, S., Yuan, L., Cao, D., Hoshino, Y., Mertens, P. P., Carner, G. R. & other authors (2010). Simian rotaviruses possess divergent gene constellations that originated from interspecies transmission and reassortment. J Virol 84, 2013-2026.
33. Matthijnssens, J., Ciarlet, M., McDonald, S. M., Attoui, H., Bányai, K., Brister, J. R., Buesa, J., Esona, M. D., Estes, M. K. & other authors (2011). Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156, 1397-1413.
34. McDonald, S. M., McKell, A. O., Rippinger, C. M., McAllen, J. K., Akopov, A., Kirkness, E. F., Payne, D. C., Edwards, K. M., Chappell, J. D. & Patton, J. T. (2012). Diversity and relationships of cocirculating modern human rotaviruses revealed using large-scale comparative genomics. J Virol 86, 9148-9162.
35. Midgley, S. E. K., Bányai, K., Buesa, J., Halaihel, N., Hjulsager, C. K., Jakab, F., Kaplon, J., Larsen, L. E., Monini, M. & other authors (2012). Diversity and zoonotic potential of rotaviruses in swine and cattle across Europe. Vet Microbiol 156, 238-245.
36. Monini, M., Cappuccini, F., Battista, P., Falcone, E., Lavazza, A. & Ruggeri, F. M. (2008). Molecular characterization of bovine rotavirus strains circulating in northern Italy, 2003-2005. Vet Microbiol 129, 384-389.
37. Mukherjee, A., Ghosh, S., Bagchi, P., Dutta, D., Chattopadhyay, S., Kobayashi, N. & Chawla-Sarkar, M. (2011). Full genomic analyses of human rotavirus G4P[4], G4P[6], G9P[19] and G10P[6] strains from North-eastern India: evidence for interspecies transmission and complex reassortment events. Clin Microbiol Infect 17, 1343-1346.
38. Naghipour, M., Nakagomi, T. & Nakagomi, O. (2008). Issues with reducing the rotavirus-associated mortality by vaccination in developing countries. Vaccine 26, 3236-3241.
39. Page, N., Esona, M., Seheri, M., Nyangao, J., Bos, P., Mwenda, J. & Steele, D. (2010). Characterization of genotype G8 strains from Malawi, Kenya, and South Africa. J Med Virol 82, 2073-2081.
40. Parashar, U. D., Burton, A., Lanata, C., Boschi-Pinto, C., Shibuya, K., Steele, D., Birmingham, M. & Glass, R. I. (2009). Global mortality associated with rotavirus disease among children in 2004. J Infect Dis 200 (Suppl 1), S9-S15.
41. Pietsch, C., Petersen, L., Patzer, L. & Liebert, U. G. (2009). Molecular characteristics of German G8P[4] rotavirus strain GER1H-09 suggest that a genotyping and subclassification update is required for G8. J Clin Microbiol 47, 3569-3576.
42. 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.
43. Suzuki, Y., Sanekata, T., Sato, M., Tajima, K., Matsuda, Y. & Nakagomi, O. (1993). Relative frequencies of G (VP7) and P (VP4) serotypes determined by polymerase chain reaction assays among Japanese bovine rotaviruses isolated in cell culture. J Clin Microbiol 31, 3046-3049.
44. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731-2739.
45. Tate, J. E., Patel, M. M., Steele, A. D., Gentsch, J. R., Payne, D. C., Cortese, M. M., Nakagomi, O., Cunliffe, N. A., Jiang, B. & other authors (2010). Global impact of rotavirus vaccines. Expert Rev Vaccines 9, 395-407.
46. Tate, J. E., Burton, A. H., Boschi-Pinto, C., Steele, A. D., Duque, J., Parashar, U. D. & WHO-coordinated Global Rotavirus Surveillance Network (2012). 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 12, 136-141.
47. Todd, S., Page, N. A., Duncan Steele, A., Peenze, I. & Cunliffe, N. A. (2010). Rotavirus strain types circulating in Africa: Review of studies published during 1997-2006. J Infect Dis 202 (Suppl), S34-S42.
48. World Health Organization (2009). Meeting of the immunization Strategic Advisory Group of Experts, April 2009-conclusions and recommendations. Wkly Epidemiol Rec 84, 220-236.
49. Xie, J.X., Duan, Z. J., Li, D.D., Li, B.W., Lan, B., Li, Y. Q., Kong, X. Y., Zhang, Q. & Li, J. (2010). [Detection of bovine rotavirus G10P[11] in a dairy farm in Daqing, China]. Bing Du Xue Bao 26, 407-409. (In Chinese)
50. Zeller, M., Heylen, E., De Coster, S., Van Ranst, M. & Matthijnssens, J. (2012). Full genome characterization of a porcine-like human G9P[6] rotavirus strain isolated from an infant in Belgium. Infect Genet Evol 12, 1492-1500.