The VP8* domain of neonatal rotavirus strain G10P[11] binds to type II precursor glycans

Journal of Virology

Volumn 87, Issue 13, 2013, Pages 7255-7264

  Ramani, Sasirekha ^a   Cortes Penfield, Nicolas W ^a   Hu, Liya ^a   Crawford, Sue E ^a   Czako , Rita ^a   Smith, David F ^b   Kang, Gagandeep ^c   Ramig, Robert F ^a   Le Pendu, Jacques ^d   Prasad, B V Venkataram ^a   Estes, Mary K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHRISTIAN MEDICAL COLLEGE   (India)

^d UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; GLYCAN; NONSTRUCTURAL PROTEIN 1; PROTEIN VP4; PROTEIN VP8; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; CAPSID PROTEIN; N ACETYLNEURAMINIC ACID; POLYSACCHARIDE; VP4 PROTEIN, ROTAVIRUS;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENOTYPE; HEMAGGLUTINATION TEST; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; ROTAVIRUS; VIRAL TROPISM; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS STRAIN; VIRUS TITRATION; ANIMAL; CATTLE; CHO CELL; CRICETULUS; GENETICS; HAMSTER; METABOLISM; NEWBORN; NEWBORN DISEASE; PROTEIN TERTIARY STRUCTURE; ROTAVIRUS INFECTION; VIROLOGY; VIRUS ATTACHMENT;

ANIMALS; CAPSID PROTEINS; CATTLE; CHO CELLS; CRICETINAE; CRICETULUS; HEMAGGLUTINATION TESTS; HUMANS; INFANT, NEWBORN; INFANT, NEWBORN, DISEASES; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES; PROTEIN STRUCTURE, TERTIARY; ROTAVIRUS; ROTAVIRUS INFECTIONS; VIRUS ATTACHMENT;

MLCS; MLOWN;

EID: 84880350145     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03518-12     Document Type: Article

References (40)

1. Stanley P, Cummings RD. 2009. Structures common to different glycans, p 175-198. In Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME (ed), Essentials in glycobiology, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Blanchard H, Yu X, Coulson BS, von Itzstein M. 2007. Insight into host cell carbohydrate-recognition by human and porcine rotavirus from crystal structures of the virion spike associated carbohydrate-binding domain (VP8*). J. Mol. Biol. 367:1215-1226.
3. Ciarlet M, Estes MK. 1999. Human and most animal rotavirus strains do not require the presence of sialic acid on the cell surface for efficient infectivity. J. Gen. Virol. 80(Pt 4):943-948.
4. Dormitzer PR, Sun ZY, Wagner G, Harrison SC. 2002. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J. 21:885-897.
5. Monnier N, Higo-Moriguchi K, Sun ZY, Prasad BV, Taniguchi K, Dormitzer PR. 2006. High-resolution molecular and antigen structure of the VP8* core of a sialic acid-independent human rotavirus strain. J. Virol. 80:1513-1523.
6. Haselhorst T, Fleming FE, Dyason JC, Hartnell RD, Yu X, Holloway G, Santegoets K, Kiefel MJ, Blanchard H, Coulson BS, von Itzstein M. 2009. Sialic acid dependence in rotavirus host cell invasion. Nat. Chem. Biol. 5:91-93.
7. Hu L, Crawford SE, Czako R, Cortes-Penfield NW, Smith DF, Le Pendu J, Estes MK, Prasad BVV. 2012. Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485:256-259.
8. Huang P, Xia M, Tan M, Zhong W, Wei C, Wang L, Morrow A, Jiang X. 2012. Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J. Virol. 86:4833-4843.
9. Liu Y, Huang P, Tan M, Biesiada J, Meller J, Castello AA, Jiang B, Jiang X. 2012. Rotavirus VP8*: phylogeny, host range and interaction with HBGAs. J. Virol. 86:9899-9910.
10. Flores J, Sears J, Green KY, Perez-Schael I, Morantes A, Daoud G, Gorziglia M, Hoshino Y, Chanock RM, Kapikian AZ. 1988. Genetic stability of rotaviruses recovered from asymptomatic neonatal infections. J. Virol. 62:4778-4781.
11. Haffejee IE. 1991. Neonatal rotavirus infections. Rev. Infect. Dis. 13:957-962.
12. Estes MK, Kapikian AZ. 2007. Rotaviruses, p 1917-1974. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
13. Varshney B, Jagannath MR, Vethanayagam RR, Kodhandharaman S, Jagannath HV, Gowda K, Singh DK, Rao CD. 2002. Prevalence of, and antigenic variation in, serotype G10 rotaviruses and detection of serotype G3 strains in diarrheic calves: implications for the origin of G10P11 or P11 type reassortant asymptomatic strains in newborn children in India. Arch. Virol. 147:143-165.
14. Vethanayagam RR, Ananda Babu M, Nagalaxmi KS, Maiya PP, Venkatesh HA, Purohit S, Behl R, Bhan MK, Ward RL, Greenberg HB, Durga Rao C. 2004. Possible role of neonatal infection with the asymp-tomatic reassortant rotavirus (RV) strain I321 in the decrease in hospital admissions for RV diarrhea, Bangalore, India, 1988-1999. J. Infect. Dis. 189:2282-2289.
15. Gulati BR, Nakagomi O, Koshimura Y, Nakagomi T, Pandey R. 1999. Relative frequencies of G and P types among rotaviruses from Indian diarrheic cow and buffalo calves. J. Clin. Microbiol. 37:2074-2076.
16. Ramani S, Sowmyanarayanan TV, Gladstone BP, Bhowmick K, Asirvatham JR, Jana AK, Kuruvilla KA, Kumar M, Gibikote S, Kang G. 2008. Rotavirus infection in the neonatal nurseries of a tertiary care hospital in India. Pediatr. Infect. Dis. J. 27:719-723.
17. Sowmyanarayanan TV, Ramani S, Sarkar R, Arumugam R, Warier JP, Moses PD, Simon A, Agarwal I, Bose A, Arora R, Kang G. 2012. Severity Neonatal Rotavirus VP8* Binds Type II Precursor of rotavirus gastroenteritis in Indian children requiring hospitalization. Vaccine 30(Suppl 1):A167-A172.
18. Banerjee I, Gladstone BP, Le Fevre AM, Ramani S, Iturriza-Gomara M, Gray JJ, Brown DW, Estes MK, Muliyil JP, Jaffar S, Kang G. 2007. Neonatal infection with G10P[11] rotavirus did not confer protection against subsequent rotavirus infection in a community cohort in Vellore, South India. J. Infect. Dis. 195:625-632.
19. Gladstone BP, Ramani S, Mukhopadhya I, Muliyil J, Sarkar R, Rehman AM, Jaffar S, Gomara MI, Gray JJ, Brown DW, Desselberger U, Crawford SE, John J, Babji S, Estes MK, Kang G. 2011. Protective effect of natural rotavirus infection in an Indian birth cohort. N. Engl. J. Med. 365:337-346.
20. Ramani S, Iturriza-Gomara M, Jana AK, Kuruvilla KA, Gray JJ, Brown DW, Kang G. 2009. Whole genome characterization of reassortant G10P[11] strain (N155) from a neonate with symptomatic rotavirus infection: identification of genes of human and animal rotavirus origin. J. Clin. Virol. 45:237-244.
21. Bhandari N, Sharma P, Taneja S, Kumar T, Rongsen-Chandola T, Appaiahgari MB, Mishra A, Singh S, Vrati S. 2009. A dose-escalation safety and immunogenicity study of live attenuated oral rotavirus vaccine 116E in infants: a randomized, double-blind, placebo-controlled trial. J. Infect. Dis. 200:421-429.
22. Cicirello HG, Das BK, Gupta A, Bhan MK, Gentsch JR, Kumar R, Glass RI. 1994. High prevalence of rotavirus infection among neonates born at hospitals in Delhi, India: predisposition of newborns for infection with unusual rotavirus. Pediatr. Infect. Dis. J. 13:720-724.
23. Das BK, Gentsch JR, Hoshino Y, Ishida S, Nakagomi O, Bhan MK, Kumar R, Glass RI. 1993. Characterization of the G serotype and genogroup of New Delhi newborn rotavirus strain 116E. Virology 197:99-107.
24. Gentsch JR, Das BK, Jiang B, Bhan MK, Glass RI. 1993. Similarity of the VP4 protein of human rotavirus strain 116E to that of the bovine B223 strain. Virology 194: 424-430.
25. Kang G, Arora R, Chitambar SD, Deshpande J, Gupte MD, Kulkarni M, Naik TN, Mukherji D, Venkatasubramaniam S, Gentsch JR, Glass RI, Parashar UD. 2009. Multicenter, hospital-based surveillance of rotavirus disease and strains among Indian children aged Universal-GreekwithMathPi.-1.H110215 years. J. Infect. Dis. 200(Suppl 1):S147-S153.
26. Alvarez RA, Blixt O. 2006. Identification of ligand specificities for glycan binding proteins using glycan arrays, p. In Fukuda M (ed), Glycobiology. Elsevier Academic Press, San Diego, CA.
27. Thorpe SJ, Boult CE, Stevenson FK, Scott ML, Sutherland J, Spellerberg MB, Natvig JB, Thompson KM. 1997. Cold agglutinin activity is common among human monoclonal IgM Rh system antibodies using the V4-34 heavy chain variable gene segment. Transfusion 37:1111-1116.
28. Guillon P, Clement M, Sebille V, Rivain JG, Chou CF, Ruvoen-Clouet N, Le Pendu J. 2008. Inhibition of the interaction between the SARS-CoV spike protein and its cellular receptor by anti-histo-blood group antibodies. Glycobiology 18:1085-1093.
29. Chen D, Burns JW, Estes MK, Ramig RF. 1989. Phenotypes of rotavirus reassortants depend upon the recipient genetic background. Proc. Natl. Acad. Sci. U.S.A. 86:3743-3747.
30. Chen DY, Estes MK, Ramig RF. 1992. Specific interactions between rotavirus outer capsid proteins VP4 and VP7 determine expression of a cross-reactive, neutralizing VP4-specific epitope. J. Virol. 66:432-439.
31. Hutson AM, Atmar RL, Marcus DM, Estes MK. 2003. Norwalk virus-like particle hemagglutination by binding to H histo-blood group antigens. J. Virol. 77:405-415.
32. North SJ, Huang HH, Sundaram S, Jang-Lee J, Etienne AT, Trollope A, Chalabi S, Dell A, Stanley P, Haslam SM. 2010. Glycomics profiling of Chinese hamster ovary cell glycosylation mutants reveals N-glycans of a novel size and complexity. J. Biol. Chem. 285:5759-5775.
33. Palombo EA, Bishop RF. 1994. Genetic analysis of NSP1 genes of human rotaviruses isolated from neonates with asymptomatic infection. J. Gen. Virol. 75(Pt 12):3635-3639.
34. Biol-N'garagba MC, Louisot P. 2003. Regulation of the intestinal glycoprotein glycosylation during postnatal development: role of hormonal and nutritional factors. Biochimie 85:331-352.
35. Fukai K, Maeda Y, Fujimoto K, Itou T, Sakai T. 2002. Changes in the prevalence of rotavirus G and P types in diarrheic calves from the Kagoshima Prefecture in Japan. Vet. Microbiol. 86:343-349.
36. Reidy N, Lennon G, Fanning S, Power E, òShea H. 2006. Molecular characterisation and analysis of bovine rotavirus strains circulating in Ireland 2002-2004. Vet. Microbiol. 117.242-247.
37. Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, Steele D, Birmingham M, Glass RI. 2009. Global mortality associated with rotavirus disease among children in 2004. J. Infect. Dis. 200(Suppl 1):S9-S15.
38. Armah GE, Sow SO, Breiman RF, Dallas MJ, Tapia MD, Feikin DR, Binka FN, Steele AD, Laserson KF, Ansah NA, Levine MM, Lewis K, Coia ML, Attah-Poku M, Ojwando J, Rivers SB, Victor JC, Nyambane G, Hodgson A, Schodel F, Ciarlet M, Neuzil KM. 2010. Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in sub-Saharan Africa: a randomised, double-blind, placebo-controlled trial. Lancet 376:606-614.
39. Madhi SA, Cunliffe NA, Steele D, Witte D, Kirsten M, Louw C, Ngwira B, Victor JC, Gillard PH, Cheuvart BB, Han HH, Neuzil KM. 2010. Effect of human rotavirus vaccine on severe diarrhea in African infants. N. Engl. J. Med. 362:289-298.
40. Zaman K, Dang DA, Victor JC, Shin S, Yunus M, Dallas MJ, Podder G, Vu DT, Le TP, Luby SP, Le HT, Coia ML, Lewis K, Rivers SB, Sack DA, Schodel F, Steele AD, Neuzil KM, Ciarlet M. 2010. Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: a randomised, double-blind, placebo-controlled trial. Lancet 376:615-623.