Genetic diversity in three bovine-like human G8P[14] and G10P[14] rotaviruses suggests independent interspecies transmission events

Journal of General Virology

Volumn 96, Issue 5, 2015, Pages 1161-1168

  Medici, Maria Cristina ^a   Tummolo, Fabio ^a   Bonica, Melisa Berenice ^a   Heylen, Elisabeth ^b   Zeller, Mark ^b   Calderaro, Adriana ^a   Matthijnssens, Jelle ^b  

^a UNIVERSITY OF PARMA   (Italy)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN VP7; VIRUS RNA;

ACUTE GASTROENTERITIS; ANIMAL VIRUS; ARTICLE; BOVINE; GENE SEQUENCE; GENETIC REASSORTMENT; GENETIC VARIABILITY; GENOME ANALYSIS; HUMAN; ITALY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAVIRUS; ROTAVIRUS INFECTION; SEQUENCE ALIGNMENT; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; CASE REPORT; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; GENOTYPE; INFANT; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; PHYLOGENY; PRESCHOOL CHILD; SEQUENCE HOMOLOGY; TRANSMISSION; VIROLOGY; VIRUS GENOME; ZOONOSIS;

ANIMALIA; BOVINAE; ROTAVIRUS; ROTAVIRUS A;

ANIMALS; CHILD, PRESCHOOL; CLUSTER ANALYSIS; GENETIC VARIATION; GENOME, VIRAL; GENOTYPE; HUMANS; INFANT; ITALY; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, VIRAL; ROTAVIRUS; ROTAVIRUS INFECTIONS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; ZOONOSES;

EID: 84930159136     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.000055     Document Type: Article

References (43)

1. Bányai, K., Gentsch, J. R., Griffin, D. D., Holmes, J. L., Glass, R. I. & Szücs, G. (2003). Genetic variability among serotype G6 human rotaviruses: identification of a novel lineage isolated in Hungary. J Med Virol 71, 124–134.
2. 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.
3. 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.
4. 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.
5. Chitambar, S. D., Arora, R., Kolpe, A. B., Yadav, M. M. & Raut, C. G. (2011). Molecular characterization of unusual bovine group A rotavirus G8P[14] strains identified in western India: emergence of P[14] genotype. Vet Microbiol 148, 384–388.
6. Cowley, D., Donato, C. M., Roczo-Farkas, S. & Kirkwood, C. D. (2013). Novel G10P[14] rotavirus strain, Northern Territory, Australia. Emerg Infect Dis 19, 1324–1327.
7. De Grazia, S., Martella, V., Rotolo, V., Bonura, F., Matthijnssens, J., Bányai, K., Ciarlet, M. & Giammanco, G. M. (2011). Molecular characterization of genotype G6 human rotavirus strains detected in Italy from 1986 to 2009. Infect Genet Evol 11, 1449–1455.
8. De Grazia, S., Bonura, F., Colomba, C., Cascio, A., Di Bernardo, F., Collura, A., Terranova, D. M., Martella, V. & Giammanco, G. M. (2014). Data mining from a 27-years rotavirus surveillance in Palermo, Italy. Infect Genet Evol 28, 377–384.
9. Degiuseppe, J. I., Beltramino, J. C., Millán, A., Stupka, J. A. & Parra, G. I. (2013). Complete genome analyses of G4P[6] rotavirus detected in Argentinean children with diarrhoea provides evidence of interspecies transmission from swine. Clin Microbiol Infect 19, e367–e371.
10. Dennis, F. E., Fujii, Y., Haga, K., Damanka, S., Lartey, B., Agbemabiese, C. A., Ohta, N., Armah, G. E. & Katayama, K. (2014). Identification of novel Ghanaian G8P[6] human–bovine reassortant rotavirus strain by next generation sequencing. PLoS ONE 9, e100699.
11. Donato, C. M., Manuelpillai, N. M., Cowley, D., Roczo-Farkas, S., Buttery, J. P., Crawford, N. W. & Kirkwood, C. D. (2014). Genetic characterization of a novel G3P[14] rotavirus strain causing gastroenteritis in 12 year old Australian child. Infect Genet Evol 25, 97–109.
12. El Sherif, M., Esona, M. D., Wang, Y., Gentsch, J. R., Jiang, B., Glass, R. I., Baker, S. A. & Klena, J. D. (2011). Detection of the first G6P[14] human rotavirus strain from a child with diarrhea in Egypt. Infect Genet Evol 11, 1436–1442.
13. Esona, M. D., Geyer, A., Page, N., Trabelsi, A., Fodha, I., Aminu, M., Agbaya, V. A., Tsion, B., Kerin, T. K. & other authors (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, M. K. & Greenberg, H. B. (2013). Rotaviruses. In Fields Virology, pp. 1347–1401. Edited by D. M. Knipe, P. M. Howley, J. I. Cohen, D. E. Griffin, R. A. Lamb, M. A. Martin, V. R. Racaniello & B. Roizman. Philadelphia: Williams and Wilkins.
15. Gentsch, J. R., Laird, A. R., Bielfelt, B., Griffin, D. D., Bányai, K., Ramachandran, M., Jain, V., Cunliffe, N. A., Nakagomi, O. & other authors (2005). Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis 192 (Suppl. 1), S146–S159.
16. Ghosh, S., Varghese, V., Samajdar, S., Sinha, M., Naik, T. N. & Kobayashi, N. (2007). Evidence for bovine origin of VP4 and VP7 genes of human group A rotavirus G6P[14] and G10P[14] strains. J Clin Microbiol 45, 2751–2753.
17. Ghosh, S., Gatheru, Z., Nyangao, J., Adachi, N., Urushibara, N. & Kobayashi, N. (2011). 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.
18. Ghosh, S., Urushibara, N., Chawla-Sarkar, M., Krishnan, T. & Kobayashi, N. (2013). Whole genomic analyses of asymptomatic human G1P[6], G2P[6] and G3P[6] rotavirus strains reveal intergenogroup reassortment events and genome segments of artiodactyl origin. Infect Genet Evol 16, 165–173.
19. Giammanco, G. M., Bonura, F., Zeller, M., Heylen, E., Van Ranst, M., Martella, V., Bányai, K., Matthijnssens, J. & De Grazia, S. (2014). Evolution of DS-1-like human G2P[4] rotaviruses assessed by complete genome analyses. J Gen Virol 95, 91–109.
20. 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.
21. Hu, L., Crawford, S. E., Czako, R., Cortes-Penfield, N. W., Smith, D. F., Le Pendu, J., Estes, M. K. & Prasad, B. V. (2012). Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485, 256–259.
22. Ianiro, G., Delogu, R., Bonomo, P., Castiglia, P., Ruggeri, F. M. & Fiore, L. (2014). Molecular characterization of human G8P[4] rotavirus strains in Italy: proposal of a more complete subclassification of the G8 genotype in three major lineages. Infect Genet Evol 21, 129–133.
23. Kim, H. J., Park, S. I., Ha, T. P., Jeong, Y. J., Kim, H. H., Kwon, H. J., Kang, M. I., Cho, K. O. & Park, S. J. (2010). Detection and genotyping of Korean porcine rotaviruses. Vet Microbiol 144, 274–286.
24. Liu, Y., Huang, P., Tan, M., Liu, Y., Biesiada, J., Meller, J., Castello, A. A., Jiang, B. & Jiang, X. (2012). Rotavirus VP8*: phylogeny, host range, and interaction with histo-blood group antigens. J Virol 86, 9899–9910.
25. Martella, V., Bányai, K., Matthijnssens, J., Buonavoglia, C. & Ciarlet, M. (2010). Zoonotic aspects of rotaviruses. Vet Microbiol 140, 246–255.
26. Matthijnssens, J., Ciarlet, M., Heiman, E., Arijs, I., Delbeke, T., McDonald, S. M., Palombo, E. A., Iturriza-Gó mara, M., Maes, P. & other authors (2008). 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.
27. Matthijnssens, J., Potgieter, C. A., Ciarlet, M., Parreño, V., Martella, V., Bányai, K., Garaicoechea, L., Palombo, E. A., Novo, L. & other authors (2009a). 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.
28. Matthijnssens, J., Bilcke, J., Ciarlet, M., Martella, V., Bányai, K., Rahman, M., Zeller, M., Beutels, P., Van Damme, P. & Van Ranst, M. (2009b). Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol 4, 1303–1316.
29. 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.
30. Medici, M. C., Abelli, L. A., Martella, V., Martinelli, M., Lorusso, E., Buonavoglia, C., Dettori, G. & Chezzi, C. (2007). Characterization of inter-genogroup reassortant rotavirus strains detected in hospitalized children in Italy. J Med Virol 79, 1406–1412.
31. Medici, M. C., Abelli, L. A., Martinelli, M., Dettori, G. & Chezzi, C. (2008). Molecular characterization of VP4, VP6 and VP7 genes of a rare G8P[14] rotavirus strain detected in an infant with gastroenteritis in Italy. Virus Res 137, 163–167.
32. Medici, M. C., Tummolo, F., Guerra, P., Arcangeletti, M. C., Chezzi, C., De Conto, F. & Calderaro, A. (2014). Evidence of VP7 and VP4 intra-lineage diversification in G4P[8] Italian human rotaviruses. Virus Genes 48, 361–365.
33. Mullick, S., Mukherjee, A., Ghosh, S., Pazhani, G. P., Sur, D., Manna, B., Nataro, J. P., Levine, M. M., Ramamurthy, T. & Chawla-Sarkar, M. (2013). Genomic analysis of human rotavirus strains G6P[14] and G11P[25] isolated from Kolkata in 2009 reveals interspecies transmission and complex reassortment events. Infect Genet Evol 14, 15–21.
34. Okada, N. & Matsumoto, Y. (2002). Bovine rotavirus G and P types and sequence analysis of the VP7 gene of two G8 bovine rotaviruses from Japan. Vet Microbiol 84, 297–305.
35. Papp, H., László, B., Jakab, F., Ganesh, B., De Grazia, S., Matthijnssens, J., Ciarlet, M., Martella, V. & Bányai, K. (2013). Review of group A rotavirus strains reported in swine and cattle. Vet Microbiol 165, 190–199.
36. Parreño, V., Bok, K., Fernandez, F. & Gomez, J. (2004). Molecular characterization of the first isolation of rotavirus in guanacos (Lama guanicoe). Arch Virol 149, 2465–2471.
37. Patel, M. M., Steele, D., Gentsch, J. R., Wecker, J., Glass, R. I. & Parashar, U. D. (2011). Real-world impact of rotavirus vaccination. Pediatr Infect Dis J 30 (Suppl.), S1–S5.
38. Pisanelli, G., Martella, V., Pagnini, U., De Martino, L., Lorusso, E., Iovane, G. & Buonavoglia, C. (2005). Distribution of G (VP7) and P (VP4) genotypes in buffalo group A rotaviruses isolated in Southern Italy. Vet Microbiol 110, 1–6.
39. Ruggeri, F. M., Delogu, R., Petouchoff, T., Tcheremenskaia, O., De Petris, S., Fiore, L. & RotaNet-Italy Study Group (2011). Molecular characterization of rotavirus strains from children with diarrhea in Italy, 2007–2009. J Med Virol 83, 1657–1668.
40. Santos, N. & Hoshino, Y. (2005). Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15, 29–56.
41. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30, 2725–2729.
42. Trojnar, E., Sachsenröder, J., Twardziok, S., Reetz, J., Otto, P. H. & Johne, R. (2013). Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol 94, 136–142.
43. Weinberg, G. A., Payne, D. C., Teel, E. N., Mijatovic-Rustempasic, S., Bowen, M. D., Wikswo, M., Gentsch, J. R. & Parashar, U. D. (2012). First reports of human rotavirus G8P[4] gastroenteritis in the United States. J Clin Microbiol 50, 1118–1121.