Histo-blood group antigen-binding specificities of human rotaviruses are associated with gastroenteritis but not with in vitro infection

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Barbé, Laure ^a   Le Moullac Vaidye, Béatrice ^a   Echasserieau, Klara ^a,b   Bernardeau, Karine ^a,b   Carton, Thomas ^c   Bovin, Nicolai ^d   Nordgren, Johan ^e   Svensson, Lennart ^e,f   Ruvoën Clouet, Nathalie ^a,g   Le Pendu, Jacques ^a  

^a UNIVERSITÉ D'ANGERS   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c Biofortis   (France)

^d SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^e LINKÖPING UNIVERSITY   (Sweden)

^f KAROLINSKA INSTITUTE   (Sweden)

^g LUNAM UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

3-GALACTOSYL-N-ACETYLGLUCOSAMINIDE 4-ALPHA-L-FUCOSYLTRANSFERASE; BLOOD GROUP ANTIGEN; FUCOSYLTRANSFERASE; GALACTOSIDE 2-ALPHA-L-FUCOSYLTRANSFERASE; NS35 PROTEIN, ROTAVIRUS; PROTEIN BINDING; RNA BINDING PROTEIN; VIRAL PROTEIN;

ADOLESCENT; ADULT; ANIMAL; CACO-2 CELL LINE; CHLOROCEBUS AETHIOPS; FEMALE; GASTROENTERITIS; GENETICS; HUMAN; MALE; METABOLISM; ROTAVIRUS; ROTAVIRUS INFECTION; VERO CELL LINE; VIROLOGY;

ADOLESCENT; ADULT; ANIMALS; BLOOD GROUP ANTIGENS; CACO-2 CELLS; CERCOPITHECUS AETHIOPS; FEMALE; FUCOSYLTRANSFERASES; GASTROENTERITIS; HUMANS; MALE; PROTEIN BINDING; RNA-BINDING PROTEINS; ROTAVIRUS; ROTAVIRUS INFECTIONS; VERO CELLS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 85052379262     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-31005-4     Document Type: Article

References (61)

1. Pesavento, J. B., Crawford, S. E., Estes, M. K. & Prasad, B. V. V. Rotavirus proteins: structure and assembly. Curr. Top. Microbiol. Immunol. 309, 189–219 (2006)
2. Matthijnssens, J. et al. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch. Virol. 156, 1397–1413 (2011)
3. 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. 15, 29–56 (2005)
4. Desselberger, U. Rotaviruses. Virus Res. 190, 75–96 (2014)
5. Bányai, K. et al. 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), A122–130 (2012)
6. Settembre, E. C., Chen, J. Z., Dormitzer, P. R., Grigorieff, N. & Harrison, S. C. Atomic model of an infectious rotavirus particle. EMBO J. 30, 408–416 (2011)
7. Padilla-Noriega, L., Dunn, S. J., López, S., Greenberg, H. B. & Arias, C. F. Identification of two independent neutralization domains on the VP4 trypsin cleavage products VP5* and VP8* of human rotavirus ST3. Virology 206, 148–154 (1995)
8. Lopez, S. & Arias, C. F. Early steps in rotavirus cell entry. Curr. Top. Microbiol. Immunol. 309, 39–66 (2006)
9. Zárate, S. et al. The VP5 Domain of VP4 Can Mediate Attachment of Rotaviruses to Cells. J. Virol. 74, 593–599 (2000)
10. Wolf, M., Vo, P. T. & Greenberg, H. B. Rhesus rotavirus entry into a polarized epithelium is endocytosis dependent and involves sequential VP4 conformational changes. J. Virol. 85, 2492–2503 (2011)
11. 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. 80(Pt 4), 943–948 (1999)
12. Haselhorst, T. et al. Sialic acid dependence in rotavirus host cell invasion. Nat. Chem. Biol. 5, 91–93 (2009)
13. Fleming, F. E. et al. Relative roles of GM1 ganglioside, N-acylneuraminic acids, and α2β1 integrin in mediating rotavirus infection. J. Virol. 88, 4558–4571 (2014)
14. Arias, C. F., Silva-Ayala, D., Isa, P., Díaz-Salinas, M. A. & López, S. Chapter 2. 2 - Rotavirus Attachment, Internalization, and VesicularTraffic. In ViralGastroenteritis (eds Svensson, L., Desselberger, U., Greenberg, H. B. & Estes, M. K.) 103–119 (Academic Press, https://doi.org/10.1016/B978-0-12-802241-2.00006-7 (2016)
15. Clausen, H. & Hakomori, S. ABH and related histo-blood group antigens; immunochemical differences in carrier isotypes and their distribution. Vox Sang. 56, 1–20 (1989)
16. Marionneau, S. et al. ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83, 565–573 (2001)
17. Huang, P. et al. Spike Protein VP8* of Human Rotavirus Recognizes Histo-Blood Group Antigens in a Type-Specific Manner. J. Virol. 86, 4833–4843 (2012)
18. Ma, X. et al. Binding Patterns of Rotavirus Genotypes P[4], P[6], and P[8] in China with Histo-Blood Group Antigens. PloS One 10, e0134584 (2015)
19. Sun, X. et al. Binding specificity of P[8] VP8* proteins of rotavirus vaccine strains with histo-blood group antigens. Virology 495, 129–135 (2016)
20. Zhang, X.-F. et al. P[8] and P[4] Rotavirus Infection Associated with Secretor Phenotypes Among Children in South China. Sci. Rep. 6, 34591 (2016)
21. Böhm, R. et al. Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion. Nat. Commun. 6, 5907 (2015)
22. Hu, L. et al. Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485, 256–259 (2012)
23. Liu, Y. et al. Rotavirus VP8*: Phylogeny, Host Range, and Interaction with Histo-Blood Group Antigens. J. Virol. 86, 9899–9910 (2012)
24. Imbert-Marcille, B.-M. et al. A FUT2 gene common polymorphism determines resistance to rotavirus A of the P[8] genotype. J. Infect. Dis. 209, 1227–1230 (2014)
25. Van Trang, N. et al. Association between norovirus and rotavirus infection and histo-blood group antigen types in Vietnamese children. J. Clin. Microbiol. 52, 1366–1374 (2014)
26. Nordgren, J. et al. Both Lewis and secretor status mediate susceptibility to rotavirus infections in a rotavirus genotype-dependent manner. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 59, 1567–1573 (2014)
27. Payne, D. C. et al. Epidemiologic Association Between FUT2 Secretor Status and Severe Rotavirus Gastroenteritis in Children in the United States. JAMA Pediatr. 169, 1040–1045 (2015)
28. Yang, T.-A., Hou, J.-Y., Huang, Y.-C. & Chen, C.-J. Genetic Susceptibility to Rotavirus Gastroenteritis and Vaccine Effectiveness in Taiwanese Children. Sci. Rep. 7, 6412 (2017)
29. Günaydın, G., Nordgren, J., Sharma, S. & Hammarström, L. Association of elevated rotavirus-specific antibody titers with HBGA secretor status in Swedish individuals: The FUT2 gene as a putative susceptibility determinant for infection. Virus Res. 211, 64–68 (2016)
30. Rodríguez-Díaz, J. et al. Relevance of secretor status genotype and microbiota composition in susceptibility to rotavirus and norovirus infections in humans. Sci. Rep. 7, 45559 (2017)
31. Ayouni, S. et al. Rotavirus P[8] Infections in Persons with Secretor and Nonsecretor Phenotypes, Tunisia. Emerg. Infect. Dis. 21, 2055–2058 (2015)
32. Tate, J. E. et al. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 12, 136–141 (2012)
33. Walker, C. L. F. et al. Global burden of childhood pneumonia and diarrhoea. The Lancet 381, 1405–1416 (2013)
34. Angel, J., Franco, M. A. & Greenberg, H. B. Rotavirus vaccines: recent developments and future considerations. Nat. Rev. Microbiol. 5, 529–539 (2007)
35. Glass, R. I., Parashar, U., Patel, M., Gentsch, J. & Jiang, B. Rotavirus vaccines: successes and challenges. J. Infect. 68(Suppl 1), S9–18 (2014)
36. López, C. A., Sovova, Z., van Eerden, F. J., de Vries, A. H. & Marrink, S. J. Martini Force Field Parameters for Glycolipids. J. Chem. Theory Comput. 9, 1694–1708 (2013)
37. Ruvoën-Clouet, N. et al. Increase in genogroup II.4 norovirus host spectrum by CagA-positive Helicobacter pylori infection. J. Infect. Dis. 210, 183–191 (2014)
38. Thomsson, K. A. et al. The salivary mucin MG1 (MUC5B) carries a repertoire of unique oligosaccharides that is large and diverse. Glycobiology 12, 1–14 (2002)
39. Mihalache, A. et al. Structural Characterization of Mucin O-Glycosylation May Provide Important Information to Help Prevent Colorectal Tumor Recurrence. Front. Oncol. 5 (2015)
40. Yu, Y. et al. Human milk contains novel glycans that are potential decoy receptors for neonatal rotaviruses. Mol. Cell. Proteomics MCP 13, 2944–2960 (2014)
41. Liu, Y. et al. Glycan Specificity of P[19] Rotavirus and Comparison with Those of Related P Genotypes. J. Virol. 90, 9983–9996 (2016)
42. Corvelo, T. C. O., Aguiar, D. C. F. & Sagica, F. E. S. The expression of ABH and Lewis antigens in Brazilian semi-isolated Black communities. Genet. Mol. Biol. 25, 259–263 (2002)
43. Nordgren, J., Nitiema, L. W., Ouermi, D., Simpore, J. & Svensson, L. Host genetic factors affect susceptibility to norovirus infections in Burkina Faso. PloS One 8, e69557 (2013)
44. Le Pendu, J., Lemieux, R. U. & Oriol, R. Purification of anti-Lec antibodies with specificity for beta DGal(1 replaced by 3)beta DGlcNAcO- using a synthetic immunoadsorbent. Vox Sang. 43, 188–195 (1982)
45. Daniels, G. Human Blood Groups. (Wiley, 2013)
46. Schnaar, R. L., Gerardy-Schahn, R. & Hildebrandt, H. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol. Rev. 94, 461–518 (2014)
47. Delorme, C. et al. Glycosphingolipid Binding Specificities of Rotavirus: Identification of a Sialic Acid-Binding Epitope. J. Virol. 75, 2276–2287 (2001)
48. Muchmore, E. A., Diaz, S. & Varki, A. A structural difference between the cell surfaces of humans and the great apes. Am. J. Phys. Anthropol. 107, 187–198 (1998)
49. Rougemont, Ade et al. Clinical severity and molecular characteristics of circulating and emerging rotaviruses in young children attending hospital emergency departments in France. Clin. Microbiol. Infect. 22, 737.e9–737.e15 (2016)
50. Wilmore, J. R. et al. Commensal Microbes Induce Serum IgA Responses that Protect against Polymicrobial Sepsis. Cell Host Microbe 23, 302–311.e3 (2018)
51. Rausch, P. et al. Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc. Natl. Acad. Sci. USA 108, 19030–19035 (2011)
52. Wacklin, P. et al. Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PloS One 6, e20113 (2011)
53. Tong, M. et al. Reprograming of gut microbiome energy metabolism by the FUT2 Crohn’s disease risk polymorphism. ISME J. 8, 2193–2206 (2014)
54. Turpin, W. et al. FUT2 genotype and secretory status are not associated with fecal microbial composition and inferred function in healthy subjects. Gut Microbes 1–12 10.1080/19490976.2018.1445956 (2018)
55. Davenport, E. R. et al. ABO antigen and secretor statuses are not associated with gut microbiota composition in 1,500 twins. BMC Genomics 17, 941 (2016)
56. Kazi, A. M. et al. Secretor and Salivary ABO Blood Group Antigen Status Predict Rotavirus Vaccine Take in Infants. J. Infect. Dis. 215, 786–789 (2017)
57. Bucardo, F. et al. The Lewis A phenotype is a restriction factor for Rotateq and Rotarix vaccine-take in Nicaraguan children. Sci. Rep. 8, 1502 (2018)
58. Blutt, S. E. et al. Gastrointestinal microphysiological systems. Exp. Biol. Med. Maywood NJ 242, 1633–1642 (2017)
59. Saxena, K. et al. Human Intestinal Enteroids: a New Model To Study Human Rotavirus Infection, Host Restriction, and Pathophysiology. J. Virol. 90, 43–56 (2015)
60. Rillahan, C. D. et al. Global Metabolic Inhibitors of Sialyl- and Fucosyltransferases. Nat. Chem. Biol. 8, 661–668 (2012)
61. Marionneau, S., Airaud, F., Bovin, N. V., Le Pendu, J. & Ruvoën-Clouet, N. Influence of the combined ABO, FUT2, and FUT3 polymorphism on susceptibility to Norwalk virus attachment. J. Infect. Dis. 192, 1071–1077 (2005)