Molecular and biological characterization of the 5 human-bovine rotavirus (WC3)-based reassortant strains of the pentavalent rotavirus vaccine, RotaTeq®

Virology

Volumn 403, Issue 2, 2010, Pages 111-127

  Matthijnssens, Jelle ^a   Joelsson, Daniel B ^b   Warakomski, Donald J ^b   Zhou, Tingyi ^b   Mathis, Pamela K ^b   van Maanen, Marc Henri ^b   Ranheim, Todd S ^b   Ciarlet, Max ^b  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Genome sequencing; Genotype; Reassortant; Rotavirus; Vaccine

Indexed keywords

NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4; NONSTRUCTURAL PROTEIN 5; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; PROTEIN VP4; PROTEIN VP6; PROTEIN VP7; ROTAVIRUS VACCINE;

ARTICLE; ELECTROPHORESIS; GENE SEQUENCE; GENETIC REASSORTMENT; GENETIC STABILITY; GENOTYPE; HUMAN ROTAVIRUS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN STRUCTURE; ROTAVIRUS INFECTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEROTYPE; VIRUS GENOME; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CLUSTER ANALYSIS; GENOMIC INSTABILITY; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; REASSORTANT VIRUSES; RNA, VIRAL; ROTAVIRUS; ROTAVIRUS VACCINES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; VACCINES, ATTENUATED; VIRAL PROTEINS;

BOVINAE; BOVINE ROTAVIRUS; BOVINE ROTAVIRUS STRAINS; BREDA VIRUS; HUMAN ROTAVIRUS A; ROTAVIRUS;

EID: 77953359180     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.04.004     Document Type: Article

References (80)

1. Abe M., Ito N., Morikawa S., Takasu M., Murase T., Kawashima T., Kawai Y., Kohara J., Sugiyama M. Molecular epidemiology of rotaviruses among healthy calves in Japan: isolation of a novel bovine rotavirus bearing new P and G genotypes. Virus Res. 2009, 144(1-2):250-257.
2. Arias C.F., Romero P., Alvarez V., López S. Trypsin activation pathway of rotavirus infectivity. J. Virol. 1996, 70(9):5832-5839.
3. Arista S., Giammanco G.M., De Grazia S., Colomba C., Martella V., Cascio A., Iturriza-Gómara M. G2 rotavirus infections in an infantile population of the South of Italy: variability of viral strains over time. J. Med. Virol. 2005, 77(4):587-594.
4. Arista S., Giammanco G.M., De Grazia S., Ramirez S., Lo Biundo C., Colomba C., Cascio A., Martella V. Heterogeneity and temporal dynamics of evolution of G1 human rotaviruses in a settled population. J. Virol. 2006, 80(21):10724-10733.
5. Bányai K., Gentsch J.R., Glass R.I., Uj M., Mihaly I., Szucs G. Eight-year survey of human rotavirus strains demonstrates circulation of unusual G and P types in Hungary. J. Clin. Microbiol. 2004, 42(1):393-397.
6. Bányai K., Bogdan A., Domonkos G., Kisfali P., Molnar P., Toth A., Melegh B., Martella V., Gentsch J.R., Szucs G. Genetic diversity and zoonotic potential of human rotavirus strains, 2003-2006, Hungary. J. Med. Virol. 2009, 81(2):362-370.
7. Bányai K., Martella V., Molnar P., Mihaly 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):213-215.
8. Bucardo F., Karlsson B., Nordgren J., Paniagua M., Gonzalez A., Amador J.J., Espinoza F., Svensson L. Mutated G4P[8] rotavirus associated with a nationwide outbreak of gastroenteritis in Nicaragua in 2005. J. Clin. Microbiol. 2007, 45(3):990-997.
9. Prevention of Rotavirus Gastroenteritis among Infants and Children: Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep. 58 (No. RR-2) 2009, 1-25. CDC.
10. Chan W.K., Au K.S., Estes M.K. Topography of the simian rotavirus nonstructural glycoprotein (NS28) in the endoplasmic reticulum membrane. Virology 1988, 164(2):435-442.
11. Chen D.Y., Estes M.K., Ramig R.F. Specific interactions between rotavirus outer capsid proteins VP4 and VP7 determine expression of a cross-reactive, neutralizing VP4-specific epitope. J. Virol. 1992, 66(1):432-439.
12. Ciarlet M., Estes M.K. Human and most animal rotavirus strains do not require the presence of sialic acid on the cell surface for efficient infectivity. J. Gen. Virol. 1999, 80:943-948.
13. Ciarlet M., Estes M.K. Interactions between rotavirus and gastrointestinal cells. Curr. Opin. Microbiol. 2001, 4(4):435-441.
14. Ciarlet M., Estes M.K. Rotaviruses: basic biology, epidemiology and methodologies. Encyclopedia of Environmental Microbiology 2002, 2573-2773. John Wiley & Sons, New York. G. Britton (Ed.).
15. Ciarlet M., Schödel F. Development of a rotavirus vaccine: clinical safety, immunogenicity, and efficacy of the pentavalent rotavirus vaccine, RotaTeq. Vaccine 2009, 27(Suppl. 6):G72-G81.
16. Ciarlet M., Hidalgo M., Gorziglia M., Liprandi F. Characterization of neutralization epitopes on the VP7 surface protein of serotype G11 porcine rotaviruses. J. Gen. Virol. 1994, 75:1867-1873.
17. Ciarlet M., Hoshino Y., Liprandi F. Single point mutations may affect the serotype reactivity of serotype G11 porcine rotavirus strains: a widening spectrum?. J. Virol. 1997, 71(11):8213-8220.
18. Ciarlet M., Crawford S., Barone C., Bertolotti-Ciarlet A., Ramig R.F., Estes M.K., Conner M.E. Subunit rotavirus vaccine administered parenterally to rabbits induces active protective immunity. J. Virol. 1998, 72(11):9233-9246.
19. Ciarlet M., Liprandi F., Conner M.E., Estes M.K. Species specificity and interspecies relatedness of NSP4 genetic groups by comparative NSP4 sequence analyses of animal rotaviruses. Arch. Virol. 2000, 145(2):371-383.
20. Ciarlet M., Crawford S., Estes M.K. Differential infection of polarized epithelial cell lines by sialic acid-dependent and sialic acid-independent rotavirus strains. J. Virol. 2001, 75(23):11834-11850.
21. Ciarlet M., Hyser J., Estes M.K. Sequence analysis of the VP4, VP6, VP7, and NSP4 gene products of the bovine rotavirus WC3. Virus Genes 2002, 24(2):107-118.
22. Ciarlet M., Ludert J.E., Iturriza-Gómara M., Liprandi F., Gray J., Desselberger U., Estes M.K. Initial interaction of rotavirus strains with N-acetylneuraminic (sialic) acid residues on the cell surface correlates with VP4 genotype, not species of origin. J. Virol. 2002, 76(8):4087-4095.
23. Clark H.F., Furukawa T., Bell L., Offit P.A., Perrella P., Plotkin S.A. Immune response of infants and children to low-passage bovine rotavirus (strain WC3). Am. J. Dis. Child. 1986, 140(4):350-356.
24. Clark H.F., Borian F., Bell L., Modesto K., Gouvea V., Plotkin S.A. Protective effect of WC3 vaccine against rotavirus diarrhea in infants during a predominantly serotype 1 rotavirus season. J. Infect. Dis. 1988, 158(3):570-587.
25. Clark H.F., Offit P.A., Ellis R., Eiden J., Krah D., Shaw A., Pichichero M., Treanor J., Borian F., Bell L., Plotkin S.A. The development of multivalent bovine rotavirus (strain WC3) reassortant vaccine for infants. J. Infect. Dis. 1996, 174(Suppl. 1):S73-S80.
26. Clark H.F., Burke C., Volkin D., Offit P.A., Ward R.L., Bresee J., Dennehy P., Gooch W., Malacaman E., Matson D., Walter E., Watson B., Krah D., Dallas M., Schödel F., Kaplan M., Heaton P. Safety, immunogenicity and efficacy in healthy infants of G1 and G2 human reassortant rotavirus vaccine in a new stabilizer/buffer liquid formulation. Pediatr. Infect. Dis. J 2003, 22(10):914-920.
27. Cook J.P., McCrae M.A. Sequence analysis of the guanylyltransferase (VP3) of group A rotaviruses. J. Gen. Virol. 2004, 85:929-932.
28. Crawford S., Mukherjee S., Estes M.K., Lawton J., Shaw A., Ramig R.F., Prasad B.V. Trypsin cleavage stabilizes the rotavirus VP4 spike. J. Virol. 2001, 75(13):6052-6061.
29. Domingo E., Martínez-Salas E., Sobrino F., de la Torre J., Portela A., Ortin J., López-Galindez C., Pérez-Brena P., Villanueva N., Najera R. The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance-a review. Gene 1985, 40(1):1-8.
30. Dyall-Smith M., Lazdins I., Tregear G., Holmes I.H. Location of the major antigenic sites involved in rotavirus serotype-specific neutralization. Proc. Natl. Acad. Sci. U. S. A. 1986, 83(10):3465-3468.
31. Espinola E., Amarilla A., Arbiza J., Parra G.I. Sequence and phylogenetic analysis of the VP4 gene of human rotaviruses isolated in Paraguay. Arch. Virol. 2008, 153(6):1067-1073.
32. Estes M.K., Kapikian A. Rotaviruses. 5th ed. Fields Virology 2007, 1917-1974. Kluwer Health/Lippincott, Williams and Wilkins, Philadelphia. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M. Martin, B. Roizman, S.E. Straus (Eds.).
33. Heaton P.M., Ciarlet M. Vaccines: the pentavalent rotavirus vaccine: discovery to licensure and beyond. Clin. Infect. Dis. 2007, 45(12):1618-1624.
34. Heaton P.M., Goveia M.G., Miller J., Offit P., Clark H.F. Development of a pentavalent rotavirus vaccine against prevalent serotypes of rotavirus gastroenteritis. J. Infect. Dis. 2005, 192(Suppl. 1):S17-S21.
35. Heiman E., McDonald S., Barro M., Taraporewala Z., 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):11106-11116.
36. Hoshino Y., Jones R., Kapikian A.Z. Characterization of neutralization specificities of outer capsid spike protein VP4 of selected murine, lapine, and human rotavirus strains. Virology 2002, 299(1):64-71.
37. Hua J., Mansell E., Patton J.T. Comparative analysis of the rotavirus NS53 gene: conservation of basic and cysteine-rich regions in the protein and possible stem-loop structures in the RNA. Virology 1993, 196(1):372-378.
38. Ito H., Sugiyama M., Masubuchi K., Mori Y., Minamoto N. Complete nucleotide sequence of a group A avian rotavirus genome and a comparison with its counterparts of mammalian rotaviruses. Virus Res. 2001, 75(2):123-138.
39. Jones R., Ross J., Hoshino Y. Identification of parental origin of cognate dsRNA genome segment(s) of rotavirus reassortants by constant denaturant gel electrophoresis. J. Clin. Virol. 2003, 26(3):347-354.
40. Khamrin P., Peerakome S., Tonusin S., Malasao R., Okitsu S., Mizuguchi M., Ushijima H., Maneekarn N. Changing pattern of rotavirus G genotype distribution in Chiang Mai, Thailand from 2002 to 2004: decline of G9 and reemergence of G1 and G2. J. Med. Virol. 2007, 79(11):1775-1782.
41. Kumar A., Charpilienne A., Cohen J. Nucleotide sequence of the gene encoding for the RNA binding protein (VP2) of RF bovine rotavirus. Nucleic Acids Res. 1989, 17(5):2126.
42. Kumar S., Tamura K., Jakobsen I., Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 2001, 17(12):1244-1245.
43. Lazdins I., Coulson B., Kirkwood C., Dyall-Smith M., Masendycz P., Sonza S., Holmes I.H. Rotavirus antigenicity is affected by the genetic context and glycosylation of VP7. Virology 1995, 209(1):80-89.
44. Maes P., Matthijnssens J., Rahman M., Van Ranst M. RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol. 2009, 9:238.
45. Malet I., Belnard M., Agut H., Cahour A. From RNA to quasispecies: a DNA polymerase with proofreading activity is highly recommended for accurate assessment of viral diversity. J. Virol. Methods 2003, 109(2):161-170.
46. Matsuda Y., Isegawa Y., Woode G.N., Zheng S., Kaga E., Nakagomi T., Ueda S., Nakagomi O. Two-way cross-neutralization mediated by a shared P (VP4) serotype between bovine rotavirus strains with distinct G (VP7) serotypes. J. Clin. Microbiol. 1993, 31(2):354-358.
47. Matthijnssens J., Rahman M., Martella V., Xuelei Y., De Vos S., De Leener K., Ciarlet M., Buonavoglia C., Van Ranst M. Full genomic analysis of human rotavirus strain B4106 and lapine rotavirus strain 30/96 provides evidence for interspecies transmission. J. Virol. 2006, 80(8):3801-3810.
48. Matthijnssens J., Rahman M., Yang X., Delbeke T., Arijs I., Kabue J.P., Muyembe J.J., Van Ranst M. G8 rotavirus strains isolated in the Democratic Republic of Congo belong to the DS-1-like genogroup. J. Clin. Microbiol. 2006, 44(5):1801-1809.
49. 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(7):3204-3219.
50. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Bányai K., Estes M.K., Gentsch J.R., Iturriza-Gómara M., Kirkwood C.D., Martella V., Mertens P., Nakagomi O., Patton J.T., Ruggeri F., Saif L.J., Santos N., Steyer A., Taniguchi K., Desselberger U., Van Ranst M. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 2008, 153(8):1621-1629.
51. Matthijnssens J., Rahman M., Ciarlet M., Van Ranst M. Emerging human rotavirus genotypes. Viruses in the Environment 2008, 171-219. Research Signpost, Trivandrum, India. E.A. Palombo, C.D. Kirkwood (Eds.).
52. Matthijnssens J., Rahman M., Van Ranst M. Two out of the 11 genes of an unusual human G6P[6] rotavirus isolate are of bovine origin. J. Gen. Virol. 2008, 89:2630-2635.
53. Matthijnssens J., Bilcke J., Ciarlet M., Martella V., Bányai K., Rahman M., Zeller M., Beutels P., Van Damme P., Van Ranst M. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol. 2009, 4:1303-1316.
54. 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 belonging to the mammalian order of Artiodactyla?. J. Virol. 2009, 83(7):2917-2929.
55. Matthijnssens J., Taraporewala Z., Yang H., Rao S., Yuan L., Cao D., Hoshino Y., Mertens P., Carner G., McNeal M., Sestak K., Van Ranst M., Patton J.T. Simian rotaviruses possess divergent gene constellations originating from interspecies transmission and reassortment. J. Virol. 2009, 84(4):2013-2026.
56. Mattion N.M., Cohen J., Aponte C., Estes M.K. Characterization of an oligomerization domain and RNA-binding properties on rotavirus nonstructural protein NS34. Virology 1992, 190(1):68-83.
57. McClain B., Settembre E., Temple B., Bellamy A.R., Harrison S.C. X-ray crystal structure of the rotavirus inner capsid particle at 3.8 A resolution. J. Mol. Biol. 2010, 39(7(2)):587-599.
58. McDonald S., Matthijnssens J., McAllen J., Hine E., Overton L., Wang S., Lemey P., Zeller M., Van Ranst M., Spiro D., Patton J.T. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog. 2009, 5(10):e1000634. (Electronic publication 2009 Oct 23).
59. Mitchell D.B., Both G.W. Completion of the genomic sequence of the simian rotavirus SA11: nucleotide sequences of segments 1, 2, and 3. Virology 1990, 177(1):324-331.
60. Offit P., Clark H.F., Ward R.L. Current state of development of human rotavirus vaccines. Viral gastroenteritis 2003, 345-356. Elsevier Science B. V., Amsterdam, Holland. U. Desselberger, J.J. Gray (Eds.).
61. Parashar U.D., Gibson C.J., Bresse J.S., Glass R.I. Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis. 2006, 12(2):304-306.
62. Parra G., Bok K., Martínez V., Russomando G., Gómez J. Molecular characterization and genetic variation of the VP7 gene of human rotaviruses isolated in Paraguay. J. Med. Virol. 2005, 77(4):579-586.
63. Patton J.T., Salter-Cid L., Kalbach A., Mansell E., Kattoura M. Nucleotide and amino acid sequence analysis of the rotavirus nonstructural RNA-binding protein NS35. Virology 1993, 192(2):438-446.
64. Paul S., Kobayashi N., Nagashima S., Ishino M., Watanabe S., Alam M.M., Ahmed M., Hossain M., Naik T.N. Phylogenetic analysis of rotaviruses with genotypes G1, G2, G9 and G12 in Bangladesh: evidence for a close relationship between rotaviruses from children and adults. Arch. Virol. 2008, 153(11):1999-2012.
65. Rahman M., Matthijnssens J., Yang X., Delbeke T., Arijs I., Taniguchi K., Iturriza-Gómara M., Iftekharuddin N., Azim T., Van Ranst M. Evolutionary history and global spread of the emerging G12 human rotaviruses. J. Virol. 2007, 81(5):2382-2390.
66. 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(1):29-56.
67. Schumann T., Hotzel H., Otto P., Johne R. Evidence of interspecies transmission and reassortment among avian group A rotaviruses. Virology 2009, 386(2):334-343.
68. Small C., Barro M., Brown T., Patton J.T. Genome heterogeneity of SA11 rotavirus due to reassortment with "O" agent. Virology 2007, 359(2):415-424.
69. Snodgrass D.R., Hoshino Y., Fitzgerald T.A., Smith M., Browning G.F., Gorziglia M. Identification of four VP4 serological types (P serotypes) of bovine rotavirus using viral reassortants. J. Gen. Virol. 1992, 73:2319-2325.
70. Solberg O.D., Hasing M.E., Trueba G., Eisenberg J.N. Characterization of novel VP7, VP4, and VP6 genotypes of a previously untypeable group A rotavirus. Virology 2009, 385(1):58-67.
71. Stirzaker S.C., Whitfeld P.L., Christie D.L., Bellamy A.R., Both G.W. Processing of rotavirus glycoprotein VP7: implications for the retention of the protein in the endoplasmic reticulum. J. Cell. Biol. 1987, 105:2897-2903.
72. Taniguchi K., Kojima K., Kobayashi N., Urasawa T., Urasawa S. Structure and function of rotavirus NSP1. Arch. Virol. Suppl. 1996, 12:53-58.
73. Trinh Q.D., Nguyen T., Phan T.G., Khamrin P., Yan H., Hoang P.L., Maneekarn N., Li Y., Yagyu F., Okitsu S., Ushijima H. Sequence analysis of the VP7 gene of human rotavirus G1 isolated in Japan, China, Thailand, and Vietnam in the context of changing distribution of rotavirus G-types. J. Med. Virol. 2007, 79(7):1009-1016.
74. Trinh Q.D., Pham N.T., Nguyen T., Phan T., Khamrin P., Yan H., Hoang P., Maneekarn N., Li Y., Kozlov V., Kozlov A., Okitsu S., Ushijima H. Amino acid substitutions in the VP7 protein of human rotavirus G3 isolated in China, Russia, Thailand, and Vietnam during 2001-2004. J. Med. Virol. 2007, 79(10):1611-1616.
75. Trojnar E., Otto P., Johne R. The first complete genome sequence of a chicken group A rotavirus indicates independent evolution of mammalian and avian strains. Virology 2009, 386:325-333.
76. Tsugawa T., Hoshino Y. 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 2008, 230(2):344-353.
77. Ursu K., Kisfali P., Rigo D., Ivanics E., Erdelyi K., Dan A., Melegh B., Martella V., Bányai K. Molecular analysis of the VP7 gene of pheasant rotaviruses identifies a new genotype, designated G23. Arch. Virol. 2009, 154:1365-1369.
78. Vesikari T., Matson D.O., Dennehy P., Van Damme P., Santosham M., Rodriguez Z., Dallas M.J., Heyse J.F., Goveia M.G., Black S.B., Shinefield H.R., Christie C.D., Ylitalo S., Itzler R.F., Coia M.L., Onorato M.T., Adeyi B.A., Marshall G.S., Gothefors L., Campens D., Karvonen A., Watt J.P., O'Brien K.L., DiNubile M., Clark H.F., Boslego J., Offit P.A., Heaton P.M. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N. Engl. J. Med. 2006, 354(1):23-33.
79. Wang Y., Kobayashi N., Zhou D., Yang Z.Q., Zhou X., Peng J.S., Zhu Z.R., Zhao D.F., Liu M.Q., Gong J. Molecular epidemiologic analysis of group A rotaviruses in adults and children with diarrhea in Wuhan city, China, 2000-2006. Arch. Virol. 2007, 152(4):669-685.
80. Wang Y., Kobayashi N., Zhou X., Nagashima S., Zhu Z.R., Peng J., Liu M.Q., Hu Q., Zhou D.J., Watanabe S., Ishino M. Phylogenetic analysis of rotaviruses with predominant G3 and emerging G9 genotypes from adults and children in Wuhan, China. J. Med. Virol. 2009, 81(2):382-389.