Problems of VirologyProblems of VirologyВопросы вирусологии0507-40882411-2097Central Research Institute for Epidemiology1673210.36233/0507-4088-306pfcbazREVIEWSОБЗОРЫReview ArticleReassortant strains of Rotavirus A (Sedoreoviridae: Rotavirus: Rotavirus A): the role of animal rotaviruses in the emergence of new human rotavirus variantsРеассортантные штаммы Rotavirus A (Sedoreoviridae: Rotavirus: Rotavirus A): роль ротавирусов животных в возникновении новых вариантов ротавируса человекаhttps://orcid.org/0000-0003-4069-1427VelikzhaninaElena I.ВеликжанинаЕлена Игоревна
Russian Federation

Junior Researcher, laboratory of molecular epidemiology of viral infections

младший научный сотрудник лаборатории молекулярной эпидемиологии вирусных инфекций

www.e_velikzhanina@mail.ruhttps://orcid.org/0000-0003-3203-7863SashinaTatiana A.СашинаТатьяна Александровна
Russian Federation

PhD, Senior Researcher, laboratory of molecular epidemiology of viral infections

канд. биол. наук, старший научный сотрудник лаборатории молекулярной эпидемиологии вирусных инфекций

tatyana.sashina@gmail.comhttps://orcid.org/0000-0002-3710-6648NovikovaNadezhda A.НовиковаНадежда Алексеевна
Russian Federation

Dr. Sci., Professor, Leading Researcher, Head of the laboratory of molecular epidemiology of viral infections

д-р биол. наук, профессор, ведущий научный сотрудник, заведующая лабораторией молекулярной эпидемиологии вирусных инфекций

novikova_na@mail.ruAcademician I.N. Blokhina Nizhny Novgorod Scientific Research Institute of Epidemiology and Microbiology of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare (Rospotrebnadzor)ФБУН «Нижегородский НИИ эпидемиологии и микробиологии им. академика И.Н. Блохиной» Федеральной службы по надзору в сфере защиты прав потребителей и благополучия человека (Роспотребнадзор)Lobachevsky State University of Nizhny NovgorodНациональный исследовательский Нижегородский государственный университет им. Н.И. Лобачевского3004202570210511627032025Copyright ©; 2025, Velikzhanina E.I., Sashina T.A., Novikova N.A.Copyright ©; 2025, Великжанина Е.И., Сашина Т.А., Новикова Н.А.2025Velikzhanina E.I., Sashina T.A., Novikova N.A.Великжанина Е.И., Сашина Т.А., Новикова Н.А.https://creativecommons.org/licenses/by/4.0https://virusjour.crie.ru/jour/article/view/16732

Animal rotaviruses (RV) play a significant role in the formation of new variants of epidemiologically significant human group A rotavirus (RVA) strains.A reassortant variant of genotype G3P[8] which has been shown to originate from RV in horses and cattle currently dominates on the territory of the Russian Federation. In addition, reassortant RV variants of genotypes G3P[3], G3P[9], G6P[9], similar to RV of cats and dogs, have been sporadically identified in the world for a long time. Given the relevance of this topic, a detailed study of the AU-1-like genetic group of RVAs, whose representatives are closely related to animal RVs, particularly those found in cats and dogs, is of scientific and practical interest.

The aim of this review is to analyze published scientific data on human, feline and canine RV that belong to the AU-1-like genetic group and have been studied based on their complete genotypes.

Ротавирусы (РВ) животных играют важную роль в формировании новых вариантов эпидемически значимых штаммов Rotavirus А (РВА) человека. В настоящее время на территории Российской Федерации преобладает реассортантный вариант генотипа G3P[8], происхождение которого связано с РВ лошадей и крупного рогатого скота. Помимо этого, в мире долгое время спорадически выявляются реассортантные варианты РВА генотипов G3P[3], G3P[9], G6P[9], подобные РВ кошек и собак. Учитывая актуальность данной темы, подробное изучение AU-1-подобной геногруппы РВА, представители которой тесно связаны с РВ кошек и собак, представляет научно-практический интерес.

Цель настоящего обзора – анализ опубликованных научных данных о РВ человека, кошек и собак, входящих в состав AU-1-подобной геногруппы и изученных на основе полного генотипа.

reviewrotavirus Awhole-genome classificationAU-1-like genetic groupfeline and canine rotavirusesобзорротавирус Аполногеномная классификацияAU-1-подобная геногруппаротавирусы кошек и собакEstes M.K., Kapikian A.Z. Rotaviruses. In: Fields B.N., Knipe D.M., Howley P.M., eds. Fields’ Virology. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2007: 1917–73.Estes M.K., Kapikian A.Z. Rotaviruses. In: Fields B.N., Knipe D.M., Howley P.M., eds. Fields Virology. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2007: 1917–73.Palombo E.A. Genetic analysis of Group A rotaviruses: evidence for interspecies transmission of rotavirus genes. Virus Genes. 2002; 24(1): 11–20. https://doi.org/10.1023/a:1014073618253KU Leuven. Rotavirus classification working group: RCWG; 2024. Available at: https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification/rcwgMatthijnssens J., Heylen E., Zeller M., Rahman M., Lemey P., Van Ranst M. Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol. Biol. Evol. 2010; 27(10): 2431–6. https://doi.org/10.1093/molbev/msq137Sashina T.A., Morozova O.V., Epifanova N.V., Novikova N.A. Predominance of new G9P[8] rotaviruses closely related to Turkish strains in Nizhny Novgorod (Russia). Arch. Virol. 2017; 162(8): 2387–92. https://doi.org/10.1007/s00705-017-3364-7Martella V., Bányai K., Matthijnssens J., Buonavoglia C., Ciarlet M. Zoonotic aspects of rotaviruses. Vet. Microbiol. 2010; 140(3-4): 246–55. https://doi.org/10.1016/j.vetmic.2009.08.028Martella V., Ciarlet M., Camarda A., Pratelli A., Tempesta M., Greco G., et al. Molecular characterization of the VP4, VP6, VP7, and NSP4 genes of lapine rotaviruses identified in Italy: emergence of a novel VP4 genotype. Virology. 2003; 314(1): 358–70. https://doi.org/10.1016/s0042-6822(03)00418-5Wang Y.H., Pang B.B., Zhou X., Ghosh S., Tang W.F., Peng J.S. et al. 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: 103–12. https://doi.org/10.1016/j.meegid.2013.01.016Nakagomi O., Nakagomi T., Oyamada H., Suto T. Relative frequency of human rotavirus subgroups 1 and 2 in Japanese children with acute gastroenteritis. J. Med. Virol. 1985; 17(1): 29–34. https://doi.org/10.1002/jmv.1890170105Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Bányai K., Estes M.K., et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 2008; 153(8): 1621–9. https://doi.org/10.1007/s00705-008-0155-1Iturriza Gómara M., Wong C., Blome S., Desselberger U., Gray J. Molecular characterization of VP6 genes of human rotavirus isolates: correlation of genogroups with subgroups and evidence of independent segregation. J. Virol. 2002; 76(13): 6596–601. https://doi.org/10.1128/jvi.76.13.6596-6601.2002Nakagomi O., Nakagomi T., Akatani K., Ikegami N. Identification of rotavirus genogroups by RNA-RNA hybridization. Mol. Cell. Probes. 1989; 3(3): 251–61. https://doi.org/10.1016/0890-8508(89)90006-6Heiman E.M., McDonald S.M., Barro M., Taraporewala Z.F., Bar-Magen T., Patton J.T. Group a human rotavirus genomics: evidence that gene constellations are influenced by viral protein interactions. J. Virol. 2008; 82(22): 11106–16. https://doi.org/10.1128/JVI.01402-08Uprety T., Wang D., Li F. Recent advances in rotavirus reverse genetics and its utilization in basic research and vaccine development. Arch. Virol. 2021; 166(9): 2369–86. https://doi.org/10.1007/s00705-021-05142-7Novikova N.A., Ponomareva N.V., Novikov D.V., Prilipov A.G., Yepifanova N.V., Golitsyna L.N. Nucleotide sequence analysis of the NSP4 gene from group a rotavirus-es isolated in Nizhni Novgorod. Voprosy virusologii. 2008; 53(6): 35–9. https://elibrary.ru/kaxfub (In Russia)Новикова Н.А., Пономарева Н.В., Новиков Д.В., Прилипов А.Г., Епифанова Н.В., Голицына Л.Н. Анализ нуклеотидных последовательностей гена NSP4 ротавирусов группы A, изолированных в Нижнем Новгороде. Вопросы вирусологии. 2008; 53(6): 35–9. https://elibrary.ru/kaxfubKomoto S., Tacharoenmuang R., Guntapong R., Ide T., Tsuji T., Yoshikawa T., et al. Reassortment of human and animal rotavirus gene segments in emerging DS-1-Like G1P[8] rotavirus strains. PLoS One. 2016; 11(2): e0148416. https://doi.org/10.1371/journal.pone.0148416Morozova O.V., Sashina T.A., Epifanova N.V., Velikzhanina E.I., Novikova N.A. Phylodynamic characteristics of reassortant DS-1-like G3P[8]-strains of rotavirus type A isolated in Nizhny Novgorod (Russia). Braz. J. Microbiol. 2023; 54(4): 2867–77. https://doi.org/10.1007/s42770-023-01155-3Nakagomi T., Nakagomi O. RNA-RNA hybridization identifies a human rotavirus that is genetically related to feline rotavirus. J. Virol. 1989; 63(3): 1431–4. https://doi.org/10.1128/JVI.63.3.1431-1434.1989Flores J., Perez-Schael I., Boeggeman E., White L., Perez M., Purcell R., et al. Genetic relatedness among human rotaviruses. J. Med. Virol. 1985; 17(2): 135–43. https://doi.org/10.1002/jmv.1890170206Espejo R.T., Calderón E., González N., Salomon A., Martuscelli A., Romero P. Presence of two distinct types of rotavirus in infants and young children hospitalized with acute gastroenteritis in Mexico City, 1977. J. Infect. Dis. 1979; 139(4): 474–7. https://doi.org/10.1093/infdis/139.4.474Greenberg H., McAuliffe V., Valdesuso J., Wyatt R., Flores J., Kalica A., et al. Serological analysis of the subgroup protein of rotavirus, using monoclonal antibodies. Infect. Immun. 1983; 39(1): 91–9. https://doi.org/10.1128/iai.39.1.91-99.1983Urasawa S., Urasawa T., Taniguchi K. Genetic reassortment between two human rotaviruses having different serotype and subgroup specificities. J. Gen. Virol. 1986; 67(Pt. 8): 1551–9. https://doi.org/10.1099/0022-1317-67-8-1551Nakagomi T., Katsushima N., Nakagomi O. Relative frequency of human rotavirus subgroups I and II in relation to “short” and “long” electropherotypes of viral RNA. Ann. Inst. Pasteur Virol. 1988; 139(3): 295–300. https://doi.org/10.1016/s0769-2617(88)80043-1Nakagomi O., Isegawa Y., Ueda S., Gerna G., Sarasini A., Kaga E., et al. Nucleotide sequence comparison of the VP8* gene of rotaviruses possessing the AU-1 gene 4 allele. J. Gen. Virol. 1993; 74(Pt. 8): 1709–13. https://doi.org/10.1099/0022-1317-74-8-1709Nakagomi O., Nakagomi T. Genetic diversity and similarity among mammalian rotaviruses in relation to interspecies transmission of rotavirus. Arch. Virol. 1991; 120(1-2): 43–55. https://doi.org/10.1007/BF01310948Matthijnssens J., Van Ranst M. Genotype constellation and evolution of group A rotaviruses infecting humans. Curr. Opin. Virol. 2012; 2(4): 426–33. https://doi.org/10.1016/j.coviro.2012.04.007Gauchan P., Sasaki E., Nakagomi T., Do L.P., Doan Y.H., Mochizuki M., et al. Whole genotype constellation of prototype feline rotavirus strains FRV-1 and FRV64 and their phylogenetic relationships with feline-like human rotavirus strains. J. Gen. Virol. 2015; 96(Pt. 2): 338–50. https://doi.org/10.1099/vir.0.070771-0Mochizuki M., Nakagomi O., Shibata S. Hemagglutinin activity of two distinct genogroups of feline and canine rotavirus strains. Arch. Virol. 1992; 122(3-4): 373–81. https://doi.org/10.1007/BF01317199De Grazia S., Giammanco G.M., Potgieter C.A., Matthijnssens J., Banyai K., Platia M.A., et al. Unusual assortment of segments in 2 rare human rotavirus genomes. Emerg. Infect. Dis. 2010; 16(5): 859–62. https://doi.org/10.3201/eid1605.091826Martella V.A., Potgieter C., Lorusso E., De Grazia S., Giammanco G.M., Matthijnssens J., et al. A feline rotavirus G3P[9] carries traces of multiple reassortment events and resembles rare human G3P[9] rotaviruses. J. Gen. Virol. 2011; 92(Pt. 5): 1214–21. https://doi.org/10.1099/vir.0.027425-0Wang Y.H., Pang B.B., Zhou X., Ghosh S., Tang W.F., Peng J.S., et al. 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: 103–12. https://doi.org/10.1016/j.meegid.2013.01.016Theamboonlers A., Maiklang O., Thongmee T., Chieochansin T., Vuthitanachot V., Poovorawan Y. Complete genome analysis of a rare human G3P[9] rotavirus posing as an AU-1 like strain. Springerplus. 2013; 2: 569. https://doi.org/10.1186/2193-1801-2-569Nguyen T.H., Than V.T., Thanh H.D., Kim W. Evidence of multiple reassortment events of feline-to-human rotaviruses based on a rare human G3P[9] rotavirus isolated from a patient with acute gastroenteritis. Comp. Immunol. Microbiol. Infect. Dis. 2016; 46: 53–9. https://doi.org/10.1016/j.cimid.2016.04.003Fukuda Y., Kaoru A., Megumi H., Yuji Y., Shuhei A., Saho H., et al. Sequence analysis of a feline- and porcine-origin G3P[9] rotavirus A strain in a child with acute gastroenteritis in Japan. Arch. Virol. 2023; 168(2): 45. https://doi.org/10.1007/s00705-022-05685-3Martella V., Pratelli A., Greco G., Gentile M., Fiorente P., Tempesta M., et al. Nucleotide sequence variation of the VP7 gene of two G3-type rotaviruses isolated from dogs. Virus Res. 2001; 74(1-2): 17–25. https://doi.org/10.1016/s0168-1702(00)00230-6Lee J.B., Youn S.J., Nakagomi T., Park S.Y., Kim T.J., Song C.S., et al. Isolation, serologic and molecular characterization of the first G3 caprine rotavirus. Arch. Virol. 2003; 148(4): 643–57. https://doi.org/10.1007/s00705-002-0963-7Matthijnssens J., De Grazia S., Piessens J., Heylen E., Zeller M., Giammanco G.M., et al. Multiple reassortment and interspecies transmission events contribute to the diversity of feline, canine and feline/canine-like human group A rotavirus strains. Infect. Genet. Evol. 2011; 11(6): 1396–406. https://doi.org/10.1016/j.meegid.2011.05.007Miño S., Matthijnssens J., Badaracco A., Garaicoechea L., Zeller M., Heylen E., et al. Equine G3P[3] rotavirus strain E3198 related to simian RRV and feline/canine-like rotaviruses based on complete genome analyses. Vet. Microbiol. 2013; 161(3-4): 239–46. https://doi.org/10.1016/j.vetmic.2012.07.033He B., Yang F., Yang W., Zhang Y., Feng Y., Zhou J., et al. Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J. Virol. 2013; 87(22): 12357–66. https://doi.org/10.1128/JVI.02013-13Papp H., Mihalov-Kovács E., Dóró R., Marton S., Farkas S.L., Giammanco G.M., et al. Full-genome sequencing of a Hungarian canine G3P[3] Rotavirus A strain reveals high genetic relatedness with a historic Italian human strain. Virus Genes. 2015; 50(2): 310–5. https://doi.org/10.1007/s11262-014-1163-8Dong H., Qian Y., Nong Y., Zhang Y., Mo Z., Li R. Genomic characterization of an unusual human G3P[3] rotavirus with multiple cross-species reassortment. Bing Du Xue Bao. 2016; 32(2): 129–40. (in Chinese)Sasaki M., Orba Y., Sasaki S., Gonzalez G., Ishii A., Hang’ombe B.M., et al. Multi-reassortant G3P[3] group A rotavirus in a horseshoe bat in Zambia. J. Gen. Virol. 2016; 97(10): 2488–93. https://doi.org/10.1099/jgv.0.000591Okitsu S., Hikita T., Thongprachum A., Khamrin P., Takanashi S., Hayakawa S., et al. Detection and molecular characterization of two rare G8P[14] and G3P[3] rotavirus strains collected from children with acute gastroenteritis in Japan. Infect. Genet. Evol. 2018; 62: 95–108. https://doi.org/10.1016/j.meegid.2018.04.011Nakagomi T., Agbemabiese C.A., Nakagomi O. Full genotype constellations of six feline Rotavirus A strains isolated in Japan in the 1990s including a rare A15 NSP1 genotype. Arch. Virol. 2018; 163(8): 2257–60. https://doi.org/10.1007/s00705-018-3835-5Charoenkul K., Janetanakit T., Bunpapong N., Boonyapisitsopa S., Tangwangvivat R., Suwannakarn K., et al. Molecular characterization identifies intra-host recombination and zoonotic potential of canine rotavirus among dogs from Thailand. Transbound. Emerg. Dis. 2021; 68(3): 1240–52. https://doi.org/10.1111/tbed.13778Azevedo L.S., Costa F.F., Ghani M.B.A., Viana E., França Y., Medeiros R.S., et al. Full genotype characterization of Brazilian canine G3P[3] strains during a 10-year survey (2012-2021) of rotavirus infection in domestic dogs and cats. Arch. Virol. 2023; 168(7): 176. https://doi.org/10.1007/s00705-023-05807-5Chamsai E., Charoenkul K., Udom K., Jairak W., Chaiyawong S., Amonsin A. Genetic characterization and evidence for multiple reassortments of rotavirus A G3P[3] in dogs and cats in Thailand. Front. Vet. Sci. 2024; 11: 1415771. https://doi.org/10.3389/fvets.2024.1415771Bányai K., Martella V., Molnár P., Mihály I., Van Ranst M., Matthijnssens J. Genetic heterogeneity in human G6P[14] rotavirus strains detected in Hungary suggests independent zoonotic origin. J. Infect. 2009; 59(3): 213–5. https://doi.org/10.1016/j.jinf.2009.06.009Nordgren J., Nitiema L.W., Sharma S., Ouermi D., Traore A.S., Simpore J., et al. Emergence of unusual G6P[6] rotaviruses in children, Burkina Faso, 2009-2010. Emerg. Infect. Dis. 2012; 18(4): 589–97. https://doi.org/10.3201/eid1804.110973Ndze V.N., Esona M.D., Achidi E.A., Gonsu K.H., Doro R., Marton S., et al. Full genome characterization of human Rotavirus A strains isolated in Cameroon, 2010-2011: diverse combinations of the G and P genes and lack of reassortment of the backbone genes. Infect. Genet. Evol. 2014; 28: 537–60. https://doi.org/10.1016/j.meegid.2014.10.009Ben Hadj Fredj M., Heylen E., Zeller M., Fodha I., Benhamida-Rebai M., Van Ranst M., et al. Feline origin of rotavirus strain, Tunisia, 2008. Emerg. Infect. Dis. 2013; 19(4): 630–4. https://doi.org/10.3201/eid1904.121383Mijatovic-Rustempasic S., Roy S., Sturgeon M., Rungsrisuriyachai K., Esona M.D., Degroat D., et al. Full-genome sequence of a rare human G3P[9] rotavirus strain. Genome Announc. 2014; 2(2): e00143-14. https://doi.org/10.1128/genomeA.00143-14Jeong S., Than VT.., Lim I., Kim W. Whole-genome analysis of a rare human Korean G3P[9] rotavirus strain suggests a complex evolutionary origin potentially in evolving reassortment events between feline and bovine rotaviruses. PLoS One. 2014; 9(5): e97127. https://doi.org/10.1371/journal.pone.0097127Lestari F.B., Chandranoi K., Chuchaona W., Vongpunsawad S., Poovorawan Y. A G3P[9] rotavirus strain with an unusual genome constellation in a diarrheic cat in Thailand. Arch. Virol. 2023; 168(1): 24. https://doi.org/10.1007/s00705-022-05641-1Fukuda Y., Kusuhara H., Takai-Todaka R., Haga K., Katayama K., Tsugawa T. Human transmission and outbreaks of feline-like G6 rotavirus revealed with whole-genome analysis of G6P[9] feline rotavirus. J. Med. Virol. 2024; 96(4): e29565. https://doi.org/10.1002/jmv.29565Pietsch C., Liebert U.G. Evidence for presumable feline origin of sporadic G6P[9] rotaviruses in humans. Infect. Genet. Evol. 2018; 63: 180–94. https://doi.org/10.1016/j.meegid.2018.05.030State report «On the state of sanitary and epidemiological welfare of the population in the Russian Federation in 2017». Moscow; 2018. (in Russian)Государственный доклад «О состоянии санитарно-эпидемиологического благополучия населения в Российской Федерации в 2017 году». М.; 2018.Kiseleva V., Faizuloev E., Meskina E., Marova A., Oksanich A., Samartseva T., et al. Molecular-genetic characterization of human rotavirus A strains circulating in Moscow, Russia (2009–2014). Virol. Sin. 2018; 33(4): 304–13. https://doi.org/10.1007/s12250-018-0043-0Zhirakovskaya E.V., Tikunov A.Y., Kurilshchikov A.M., Tikunova N.V., Aksanova R.K., Sokolov S.N., et al. Genetic diversity of group A rotavirus isolates found in Western Siberia in 2007–2011. Molekulyarnaya genetika, mikrobiologiya i virusologiya. 2012; 27(4): 174–83. https://doi.org/10.3103/S0891416812040076 https://elibrary.ru/rgcgdzЖираковская Е.В., Аксанова Р.Х., Горбунова М.Г., Тикунов А.Ю., Курильщиков А.М., Соколов С.Н. и др. Генетическое разнообразие изолятов ротавирусов группы А, выявленных в Западной Сибири в 2007–2011 гг. Молекулярная генетика, микробиология и вирусология. 2012; (4): 33–41. https://elibrary.ru/rbgqibSashina T.A., Velikzhanina E.I., Morozova O.V., Epifanova N.V., Novikova N.A. Detection and full-genotype characterization of rare and reassortant rotavirus A strains in Nizhny Novgorod, European part of Russia. Arch. Virol. 2023; 168(8): 215. https://doi.org/10.1007/s00705-023-05838-yVelikzhanina E.I., Sashina T.A., Morozova O.V., Epifanova N.V., Novikova N.A. Variability of genes encoding nonstructural proteins of rotavirus А (Reoviridae: Rotavirus: Rotavirus A) genotype G9P[8] during the period of dominance in the territory of Nizhny Novgorod (central part of Russia) (2011–2020). Voprosy virusologii. 2022; 67(6): 475–86. https://doi.org/10.36233/0507-4088-143 https://elibrary.ru/oeuvma (in Russian)Великжанина Е.И., Сашина Т.А., Морозова О.В., Епифанова Н.В., Новикова Н.А. Вариабельность генов неструктурных белков ротавируса А (Reoviridae: Rotavirus: Rotavirus A) генотипа G9P[8] в период доминирования на территории Нижнего Новгорода (центральная часть России) (2011–2020). Вопросы вирусологии. 2022; 67(6): 475–86. https://doi.org/10.36233/0507-4088-143 https://elibrary.ru/oeuvma