Identification of novel and diverse rotaviruses in rodents and insectivores, and evidence of cross-species transmission into humans

Virology

Volumn 494, Issue , 2016, Pages 168-177

  Li, Kun ^a,b   Lin, Xian Dan ^c   Huang, Kai Yu ^d   Zhang, Bing ^a   Shi, Mang ^a,e   Guo, Wen Ping ^a,b   Wang, Miao Ruo ^f   Wang, Wen ^a,b   Xing, Jian Guang ^g   Li, Ming Hui ^a,b   Hong, Wang Sheng ^h   Holmes, Edward C ^a,e   Zhang, Yong Zhen ^a,b  

^a National Institute for Communicable Disease Control and Prevention   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c Wenzhou Municipal Center for Disease Control and Prevention   (China)

^d THE SECOND AFFILIATED HOSPITAL AND YUYING CHILDREN S HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

^e University of Sydney   (Australia)

^f Longquan Center for Disease Control and Prevention   (China)

^g Wencheng District Center for Disease Control and Prevention   (China)

^h Ruian Center for Disease Control and Prevention   (China)

Author keywords

Evolution; Genotype; Human infection; Reassortment; Rodents; Rotavirus; Shrews

Indexed keywords

ARTICLE; CONTROLLED STUDY; DIARRHEA; GENETIC VARIABILITY; GENOTYPE; HUMAN; INSECTIVORE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; RODENT; ROTAVIRUS; SPECIES DIVERSITY; VIRUS IDENTIFICATION; VIRUS TRANSMISSION; ANIMAL; CHILD; CHINA; CLASSIFICATION; FECES; FEMALE; GENETICS; INFANT; INSECT; MALE; MAMMAL; PRESCHOOL CHILD; ROTAVIRUS INFECTIONS; TRANSMISSION; VIROLOGY; VIRUS GENOME; ZOONOSIS;

CAPSID PROTEIN;

ANIMALS; CAPSID PROTEINS; CHILD; CHILD, PRESCHOOL; CHINA; DIARRHEA; EVOLUTION, MOLECULAR; FECES; FEMALE; GENOME, VIRAL; GENOTYPE; HUMANS; INFANT; INSECTS; MALE; MAMMALS; PHYLOGENY; RODENTIA; ROTAVIRUS; ROTAVIRUS INFECTIONS; ZOONOSES;

EID: 84963957953     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2016.04.017     Document Type: Article

References (49)

1. Bányai K., László B., Duque J., Steele A.D., Nelson E.A., Gentsch J.R., Parashar U.D. Systematic review of regional and temporal trends in global rotavirus strain diversity in the prerotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 2012, 30S:A122-A130.
2. Ben Hadj Fredj M., Heylen E., Zeller M., Fodha I., Benhamida-Rebai M., Van Ranst M., Matthijnssens J., Trabelsi A. Feline origin of rotavirus strain, Tunisia, 2008. Emerg. Infect. Dis. 2013, 19:630-634.
3. Bonica M.B., Zeller M., Van Ranst M., Matthijnssens J., Heylen E. Complete genome analysis of a rabbit rotavirus causing gastroenteritis in a human infant. Viruses 2015, 7:844-856.
4. Cowley D., Donato C.M., Roczo-Farkas S., Kirkwood C.D. Novel G10P[14] rotavirus strain, northern territory, Australia. Emerg. Infect. Dis. 2013, 19:1324-1327.
5. Dóró R., László B., Martella V., Leshem E., Gentsch J., Parashar U., Bányai K. Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: is there evidence of strain selection from vaccine pressure?. Infect. Genet. Evol. 2014, 28:446-461.
6. Estes M., Greenberg H.B. Rotaviruses. Fields Virology 2013, vol. 2:1347-1401. Lippincott, Williams and Wilkins, Philadelphia, PA. 6th ed.
7. Everest D.J., Duff J.P., Higgins R.J. Rotavirus in a wild English red squirrel (Sciurus vulgaris) identified by electron microscopy. Vet. Rec. 2011, 169:160.
8. Firth C., Bhat M., Firth M.A., Williams S.H., Frye M.J., Simmonds P., Conte J.M., Ng J., Garcia J., Bhuva N.P., Lee B., Che X., Quan P.L., Lipkin W.I. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. MBio 2014, 5. e01933-14.
9. Gautam R., Mijatovic-Rustempasic S., Roy S., Esona M.D., Lopez B., Mencos Y., Rey-Benito G., Bowen M.D. Full genomic characterization and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain detected in a sample from Guatemala. Infect. Genet. Evol. 2015, 33:206-211.
10. Gonzalez J.P., Emonet S., de Lamballerie X., Charrel R. Arenaviruses. Curr. Top. Microbiol. Immunol. 2007, 315:253-288.
11. Greenwood A.G., Sanchez S. Serological evidence of murine pathogens in wild grey squirrels (Sciurus carolinensis) in North Wales. Vet. Rec. 2002, 150:543-546.
12. Guindon S., Delsuc F., Dufayard J.F., Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods. Mol. Biol. 2009, 537:113-137.
13. Guo W.P., Lin X.D., Wang W., Tian J.H., Cong M.L., Zhang H.L., Wang M.R., Zhou R.H., Wang J.B., Li M.H., Xu J., Holmes E.C., Zhang Y.Z. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. Plos. Pathog. 2013, 9:e1003159.
14. He B., Yang F., Yang W., Zhang Y., Feng Y., Zhou J., Xie J., Feng Y., Bao X., Guo H., Li Y., Xia L., Li N., Matthijnssens J., Zhang H., Tu C. Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J. Virol. 2013, 87:12357-12366.
15. Holmes E.C., Zhang Y.Z. The evolution and emergence of hantaviruses. Curr. Opin. Virol. 2015, 10:27-33.
16. Jeong S., Than V.T., Lim I., Kim W. Whole-genome analysis of a rare human Korean G3P[9] rotavirus strain suggests a complex evolutionary origin potentially involving reassortment events between feline and bovine rotaviruses. Plos. One 2014, 9:e97127.
17. Li K., Lin X.D., Wang W., Shi M., Guo W.P., Zhang X.H., Xing J.G., He J.R., Wang K., Li M.H., Cao J.H., Jiang M.L., Holmes E.C., Zhang Y.Z. Isolation and characterization of a novel arenavirus harbored by Rodents and Shrews in Zhejiang province, China. Virology 2015, 476:37-42.
18. Li Y., Wang S.M., Zhen S.S., Chen Y., Deng W., Kilgore P.E., Wang X.Y. Diversity of rotavirus strains causing diarrhea in <5 years old Chinese children: a systematic review. Plos. One 2014, 9. e84699.
19. Linhares A.C., Pereira J.D., Nakauth C.M., Gabbay Y.B. Rotavirus infection in wild marsupials (Didelphis marsupialis) of the Amazon region. Trans. R. Soc. Trop. Med. Hyg. 1986, 80:20-24.
20. Liu N., Xu Z., Li D., Zhang Q., Wang H., Duan Z.J. Update on the disease burden and circulating strains of rotavirus in China: a systematic review and meta-analysis. Vaccine 2014, 32:4369-4375.
21. Luis A.D., Hayman D.T., O'Shea T.J., Cryan P.M., Gilbert A.T., Pulliam J.R., Mills J.N., Timonin M.E., Willis C.K., Cunningham A.A., Fooks A.R., Rupprecht C.E., Wood J.L., Webb C.T. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?. Proc. Biol. Sci. 2013, 280:20122753.
22. Martella V., Bányai K., Matthijnssens J., Buonavoglia C., Ciarlet M. Zoonotic aspects of rotaviruses. Vet. Microbiol. 2010, 140:246-255.
23. Matthijnssens J., Ciarlet M., Heiman E., Arijs I., Delbeke T., McDonald S.M., Palombo E.A., Iturriza-Gómara M., Maes P., Patton J.T., Rahman M., Van Ranst M. 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. 2008, 82:3204-3219.
24. Matthijnssens J., Ciarlet M., McDonald S.M., Attoui H., Bányai K., Brister J.R., Buesa J., Esona M.D., Estes M.K., Gentsch J.R., Iturriza-Gómara M., Johne R., Kirkwood C.D., Martella V., Mertens P.P., Nakagomi O., Parreño V., Rahman M., Ruggeri F.M., Saif L.J., Santos N., Steyer A., Taniguchi K., Patton J.T., Desselberger U., Van Ranst M. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch. Virol. 2011, 156:1397-1413.
25. Matthijnssens J., Otto P.H., Ciarlet M., Desselberger U., Van Ranst M., Johne R. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch. Virol. 2012, 157:1177-1182.
26. Matthijnssens J., Rahman M., Ciarlet M., Zeller M., Heylen E., Nakagomi T., Uchida R., Hassan Z., Azim T., Nakagomi O., Van Ranst M. Reassortment of human rotavirus gene segments into G11 rotavirus strains. Emerg. Infect. Dis. 2010, 16:625-630.
27. Matthijnssens J., Potgieter C.A., Ciarlet M., Parreño V., Martella V., Bányai K., Garaicoechea L., Palombo E.A., Novo L., Zeller M., Arista S., Gerna G., Rahman M., Van Ranst M. 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. 2009, 83:2917-2929.
28. Matthijnssens J., Van Ranst M. Genotype constellation and evolution of group A rotaviruses infecting humans. Curr. Opin. Virol. 2012, 2:426-433.
29. Medici M.C., Tummolo F., Bonica M.B., Heylen E., Zeller M., Calderaro A., Matthijnssens J. Genetic diversity in three bovine-like human G8P[14] and G10P[14] rotaviruses suggests independent interspecies transmission events. J. Gen. Virol. 2015, 96:1161-1168.
30. Meerburg B.G., Singleton G.R., Kijlstra A. Rodent-borne diseases and their risks for public health. Crit. Rev. Microbiol. 2009, 35:221-270.
31. Mihalov-Kovács E., Gellért Á., Marton S., Farkas S.L., Fehér E., Oldal M., Jakab F., Martella V., Bányai K. Candidate new rotavirus species in sheltered dogs. Hungary. Emerg. Infect. Dis 2015, 21:660-663.
32. Nan X., Jinyuan W., Yan Z., Maosheng S., Hongjun L. Epidemiological and clinical studies of rotavirus-induced diarrhea in China from 1994-2013. Hum. Vaccin. Immunother. 2014, 10:3672-3680.
33. Nordgren J., Nitiema L.W., Sharma S., Ouermi D., Traore A.S., Simpore J., Svensson L. Emergence of unusual G6P[6] rotaviruses in children, Burkina Faso, 2009-2010. Emerg. Infect. Dis. 2012, 18:589-597.
34. Posada D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
35. Rotavirus Classification Working Group (RCWG). 2015. Newly assigned genotypes. http://https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification/rcwg.
36. Sachsenröder J., Braun A., Machnowska P., Ng T.F., Deng X., Guenther S., Bernstein S., Ulrich R.G., Delwart E., Johne R. Metagenomic identification of novel enteric viruses in urban wild rats and genome characterization of a group A rotavirus. J. Gen. Virol. 2014, 95:2734-2747.
37. Santos N., Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev. Med. Virol. 2005, 15:29-56.
38. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
39. Tate J.E., Burton A.H., Boschi-Pinto C., Steele A.D., Duque J., Parashar U.D. WHO-coordinated Global Rotavirus Surveillance Network., 2012. Lancet Infect. Dis. 2008, 12:136-141. estimate of worldwiderotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis.
40. Theuns S., Heylen E., Zeller M., Roukaerts I.D., Desmarets L.M., Van Ranst M., Nauwynck H.J., Matthijnssens J. Complete genome characterization of recent and ancient Belgian pig group A rotaviruses and assessment of their evolutionary relationship with human rotaviruses. J. Virol. 2015, 89:1043-1057.
41. Trojnar E., Sachsenroder J., Twardziok S., Reetz J., Otto P.H., Johne R. Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J. Gen. Virol. 2013, 94:136-142.
42. Wang W., Lin X.D., Zhou R.H., Wang M.R., Wang C.Q., Ge S., Mei S.H., Li M.H., Shi M., Holmes E.C., Zhang Y.Z. Discovery, diversity and evolution of novel coronaviruses sampled from rodents in China. Virology 2015, 474:19-27.
43. Wang W., Wang M.R., Lin X.D., Guo W.P., Li M.H., Mei S.H., Li Z.M., Cong M.L., Jiang R.L., Zhou R.H., Holmes E.C., Plyusnin A., Zhang Y.Z. Ongoing spillover of Hantaan and Gou hantaviruses from rodents is associated with hemorrhagic fever with renal syndrome (HFRS) in China. Plos. Negl. Trop. Dis. 2013, 7:e2484.
44. Wang Y.H., Pang B.B., Zhou X., Ghosh S., Tang W.F., Peng J.S., Hu Q., Zhou D.J., Kobayashi N. Complex evolutionary patterns of two rare human G3P[9] rotavirus strains possessing a feline/canine-like H6 genotype on an AU-1-like genotype constellation. Infect. Genet. Evol. 2013, 16:103-112.
45. Wilson D.E., Reeder D.M. Mammal Species of the World. A Taxonomic and Geographic Reference 2005, 745-751. The Johns Hopkins University Press, Baltimore. 3rd ed.
46. Yoon S.W., Webby R.J., Webster R.G. Evolution and ecology of influenza A viruses. Curr. Top. Microbiol. Immunol. 2014, 385:359-375.
47. Zeller M., Rahman M., Heylen E., De Coster S., De Vos S., Arijs I., Novo L., Verstappen N., Van Ranst M., Matthijnssens J. Rotavirus incidence and genotype distribution before and after national rotavirus vaccine introduction in Belgium. Vaccine 2010, 28:7507-7513.
48. Zhang J., Duan Z., Payne D.C., Yen C., Pan X., Chang Z., Liu N., Ye J., Ren X., Tate J.E., Jiang B., Parashar U.D. Rotavirus-Specific and Overall Diarrhea Mortality in Chinese Children Younger than 5 Years; 2003 to 2012. Pediatr. Infect. Dis. J. 2015, 34:e233-e237.
49. Zhou X., Wang Y.H., Ghosh S., Tang W.F., Pang B.B., Liu M.Q., Peng J.S., Zhou D.J., Kobayashi N. Genomic characterization of G3P[6], G4P[6] and G4P[8] human rotaviruses from Wuhan, China: Evidence for interspecies transmission and reassortment events. Infect. Genet. Evol. 2015, 33:55-71.