Alternative attachment factors and internalization pathways for GIII.2 bovine noroviruses.

[en] Bovine noroviruses belong to the family Caliciviridae, genus Norovirus. Two genotypes are described and viruses genetically related to the Jena and Newbury-2 strains are classified into genotypes 1 and 2 respectively. In this study, virus-like particles (VLP) of the previously detected B309 Belgian strain, genetically related to genotype 2 bovine noroviruses, were used to investigate virus-host interactions in vitro. B309 VLP were shown to bind to several bovine cell lines. This binding was not affected by heparinase or chondroitinase treatment but was significantly inhibited by both sodium periodate, alpha-galactosidase, trypsin and phospholipase C treatment. Cell treatment by neuraminidase also moderately affected this binding. Taken together, these results show that, in addition to a galactosyl residue, sialic acid could also be involved in binding to susceptible cells. In addition, both the cholesterol-dependent pathway and macropinocytosis are used for B309 VLP internalisation by Madin-Darby Bovine Kidney cells. The data increase the knowledge on bovine norovirus cell interactions.

Disciplines :

Microbiology

Author, co-author :

Mauroy, Axel ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie vétérinaire et maladies virales animales

Gillet, Laurent ; Université de Liège - ULiège > Immunologie et vaccinologie

Mathijs, Elisabeth ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie vétérinaire et maladies virales animales

Vanderplasschen, Alain ; Université de Liège - ULiège > Immunologie et vaccinologie

Thiry, Etienne ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie vétérinaire et maladies virales animales

Language :

English

Title :

Alternative attachment factors and internalization pathways for GIII.2 bovine noroviruses.

Publication date :

2011

Journal title :

Journal of General Virology

ISSN :

0022-1317

eISSN :

1465-2099

Publisher :

Society for General Microbiology, London, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 March 2011

Statistics

Number of views

86 (9 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Baranowski, E., Ruiz-Jarabo, C. M. & Domingo, E. (2001). Evolution of cell recognition by viruses. Science 292, 1102-1105.
Bridger, J. C., Hall, G. A. & Brown, J. F. (1984). Characterization of a calici-like virus (Newbury agent) found in association with astrovirus in bovine diarrhea. Infect Immun 43, 133-138.
Cilliers, T., Willey, S., Sullivan, W. M., Patience, T., Pugach, P., Coetzer, M., Papathanasopoulos, M., Moore, J. P., Trkola, A. & Clapham, P. (2005). Use of alternate coreceptors on primary cells by two HIV-1 isolates. Virology 339, 136-144.
Crawford, S. E., Patel, D. G., Cheng, E., Berkova, Z., Hyser, J. M., Ciarlet, M., Finegold, M. J., Conner, M. E. & Estes, M. K. (2006). Rotavirus viremia and extraintestinal viral infection in the neonatal rat model. J Virol 80, 4820-4832.
Duizer, E., Schwab, K. J., Neill, F. H., Atmar, R. L., Koopmans, M. P. & Estes, M. K. (2004). Laboratory efforts to cultivate noroviruses. J Gen Virol 85, 79-87.
Gerondopoulos, A., Jackson, T., Monaghan, P., Doyle, N. & Roberts, L. O. (2010). Murine norovirus-1 cell entry is mediated through a non-clathrin-, non-caveolae-, dynamin- and cholesterol-dependent pathway. J Gen Virol 91, 1428-1438.
Girao, H., Geli, M. I. & Idrissi, F. Z. (2008). Actin in the endocytic pathway: from yeast to mammals. FEBS Lett 582, 2112-2119.
Green, K. Y. (2007). Caliciviridae: The Noroviruses. In Fields Virology, 5th edn, pp. 949-979. Edited by D. M. Knipe. Philadelphia, USA: Lippinscott Williams & Wilkins.
Han, M. G., Smiley, J. R., Thomas, C. & Saif, L. J. (2004). Genetic recombination between two genotypes of genogroup III bovine noroviruses (BoNVs) and capsid sequence diversity among BoNVs and Nebraska-like bovine enteric caliciviruses. J Clin Microbiol 42, 5214-5224.
Han, M. G., Wang, Q., Smiley, J. R., Chang, K. O. & Saif, L. J. (2005). Self-assembly of the recombinant capsid protein of a bovine norovirus (BoNV) into virus-like particles and evaluation of crossreactivity of BoNV with human noroviruses. J Clin Microbiol 43, 778-785.
Harouse, J. M., Laughlin, M. A., Pletcher, C., Friedman, H. M. & Gonzalez-Scarano, F. (1991). Entry of human immunodeficiency virus-1 into glial cells proceeds via an alternate, efficient pathway. J Leukoc Biol 49, 605-609.
Ike, A. C., Roth, B. N., Böhm, R., Pfitzner, A. J. & Marschang, R. E. (2007). Identification of bovine enteric Caliciviruses (BEC) from cattle in Baden-Württemberg. Dtsch Tierarztl Wochenschr 114, 12-15.
Jiang, X., Wang, M., Graham, D. Y. & Estes, M. K. (1992). Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J Virol 66, 6527-6532.
Jin, Q., Alkhatib, B., Cornetta, K. & Alkhatib, G. (2010). Alternate receptor usage of neuropilin-1 and glucose transporter protein 1 by the human T cell leukemia virus type 1. Virology 396, 203-212.
Khan, A. G., Pichler, J., Rosemann, A. & Blaas, D. (2007). Human rhinovirus type 54 infection via heparan sulfate is less efficient and strictly dependent on low endosomal pH. J Virol 81, 4625-4632.
Liu, B. L., Lambden, P. R., Günther, H., Otto, P., Elschner, M. & Clarke, I. N. (1999). Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. J Virol 73, 819-825.
Loret, S., Rusu, D., El Moualij, B., Taminiau, B., Heinen, E., Dandrifosse, G. & Mainil, J. (2009). Preliminary characterization of jejunocyte and colonocyte cell lines isolated by enzymatic digestion from adult and young cattle. Res Vet Sci 87, 123-132.
Macher, B. A. & Galili, U. (2008). The Gala1,3Galb1,4GlcNAc-R (a- Gal) epitope: a carbohydrate of unique evolution and clinical relevance. Biochim Biophys Acta 1780, 75-88.
Makino, A., Shimojima, M., Miyazawa, T., Kato, K., Tohya, Y. & Akashi, H. (2006). Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J Virol 80, 4482-4490.
Marsh, M. & Helenius, A. (2006). Virus entry: open sesame. Cell 124, 729-740.
Mauroy, A., Scipioni, A., Mathijs, E., Miry, C., Ziant, D., Thys, C. & Thiry, E. (2008). Noroviruses and sapoviruses in pigs in Belgium. Arch Virol 153, 1927-1931.
Mauroy, A., Scipioni, A., Mathijs, E., Saegerman, C., Mast, J., Bridger, J. C., Ziant, D., Thys, C. & Thiry, E. (2009a). Epidemiological study of bovine norovirus infection by RT-PCR and a VLP-based antibody ELISA. Vet Microbiol 137, 243-251.
Mauroy, A., Scipioni, A., Mathijs, E., Thys, C. & Thiry, E. (2009b). Molecular detection of kobuviruses and recombinant noroviruses in cattle in continental Europe. Arch Virol 154, 1841-1845.
Miller, N. & Hutt-Fletcher, L. M. (1992). Epstein-Barr virus enters B cells and epithelial cells by different routes. J Virol 66, 3409-3414.
Milnes, A. S., Binns, S. H., Oliver, S. L. & Bridger, J. C. (2007). Retrospective study of noroviruses in samples of diarrhoea from cattle, using the Veterinary Laboratories Agency's Farmfile database. Vet Rec 160, 326-330.
Negrete, O. A., Wolf, M. C., Aguilar, H. C., Enterlein, S., Wang, W., Mühlberger, E., Su, S. V., Bertolotti-Ciarlet, A., Flick, R. & Lee, B. (2006). Two key residues in ephrinB3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog 2, e7.
Nilsson, J., Rydell, G. E., Le Pendu, J. & Larson, G. (2009). Norwalk virus-like particles bind specifically to A, H and difucosylated Lewis but not to B histo-blood group active glycosphingolipids. Glycoconj J 26, 1171-1180.
Nordgren, J., Kindberg, E., Lindgren, P. E., Matussek, A. & Svensson, L. (2010). Norovirus gastroenteritis outbreak with a secretor-independent susceptibility pattern, Sweden. Emerg Infect Dis 16, 81-87.
Oliver, S. L., Asobayire, E., Charpilienne, A., Cohen, J. & Bridger, J. C. (2007). Complete genomic characterization and antigenic relatedness of genogroup III, genotype 2 bovine noroviruses. Arch Virol 152, 257-272.
Ossiboff, R. J. & Parker, J. S. (2007). Identification of regions and residues in feline junctional adhesion molecule required for feline calicivirus binding and infection. J Virol 81, 13608-13621.
Park, S. I., Jeong, C., Kim, H. H., Park, S. H., Park, S. J., Hyun, B. H., Yang, D. K., Kim, S. K., Kang, M. I. & Cho, K. O. (2007). Molecular epidemiology of bovine noroviruses in South Korea. Vet Microbiol 124, 125-133.
Perry, J. W. & Wobus, C. E. (2010). Endocytosis of murine norovirus 1 into murine macrophages is dependent on dynamin II and cholesterol. J Virol 84, 6163-6176.
Perry, J. W., Taube, S. & Wobus, C. E. (2009). Murine norovirus-1 entry into permissive macrophages and dendritic cells is pHindependent. Virus Res 143, 125-129.
Ruvoën-Clouet, N., Ganière, J. P., André-Fontaine, G., Blanchard, D. & le Pendu, J. (2000). Binding of rabbit hemorrhagic disease virus to antigens of the ABH histo-blood group family. J Virol 74, 11950-11954.
Rydell, G. E., Nilsson, J., Rodriguez-Diaz, J., Ruvoën-Clouet, N., Svensson, L., le Pendu, J. & Larson, G. (2009). Human noroviruses recognize sialyl Lewis x neoglycoprotein. Glycobiology 19, 309-320.
Scipioni, A., Mauroy, A., Vinjé, J. & Thiry, E. (2008). Animal noroviruses. Vet J 178, 32-45.
Sieczkarski, S. B. & Whittaker, G. R. (2002). Dissecting virus entry via endocytosis. J Gen Virol 83, 1535-1545.
Smith, A. E. & Helenius, A. (2004). How viruses enter animal cells. Science 304, 237-242.
Stuart, A. D. & Brown, T. D. (2006). Entry of feline calicivirus is dependent on clathrin-mediated endocytosis and acidification in endosomes. J Virol 80, 7500-7509.
Stuart, A. D. & Brown, T. D. (2007). α2,6-linked sialic acid acts as a receptor for Feline calicivirus. J Gen Virol 88, 177-186.
Tamura, M., Natori, K., Kobayashi, M., Miyamura, T. & Takeda, N. (2004). Genogroup II noroviruses efficiently bind to heparan sulfate proteoglycan associated with the cellular membrane. J Virol 78, 3817-3826.
Tan, M. & Jiang, X. (2005). Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol 13, 285-293.
Tan, M., Huang, P., Meller, J., Zhong, W., Farkas, T. & Jiang, X. (2003). Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket. J Virol 77, 12562-12571.
Taube, S., Perry, J. W., Yetming, K., Patel, S. P., Auble, H., Shu, L., Nawar, H. F., Lee, C. H., Connell, T. D. & other authors (2009). Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J Virol 83, 4092-4101.
van der Poel, W. H., van der Heide, R., Verschoor, F., Gelderblom, H., Vinjé, J. & Koopmans, M. P. (2003). Epidemiology of Norwalk-like virus infections in cattle in The Netherlands. Vet Microbiol 92, 297-309.
Vanderplasschen, A., Bublot, M., Dubuisson, J., Pastoret, P. P. & Thiry, E. (1993). Attachment of the gammaherpesvirus bovine herpesvirus 4 is mediated by the interaction of gp8 glycoprotein with heparinlike moieties on the cell surface. Virology 196, 232-240.
Villanueva, R. A., Rouillé, Y. & Dubuisson, J. (2005). Interactions between virus proteins and host cell membranes during the viral life cycle. Int Rev Cytol 245, 171-244.
Wise, A. G., Monroe, S. S., Hanson, L. E., Grooms, D. L., Sockett, D. & Maes, R. K. (2004). Molecular characterization of noroviruses detected in diarrheic stools of Michigan and Wisconsin dairy calves: circulation of two distinct subgroups. Virus Res 100, 165-177.
Woode, G. N. & Bridger, J. C. (1978). Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. J Med Microbiol 11, 441-452.
Yanagi, Y., Takeda, M., Ohno, S. & Hashiguchi, T. (2009). Measles virus receptors. Curr Top Microbiol Immunol 329, 13-30.
Zakhour, M., Ruvoën-Clouet, N., Charpilienne, A., Langpap, B., Poncet, D., Peters, T., Bovin, N. & le Pendu, J. (2009). The aGal epitope of the histo-blood group antigen family is a ligand for bovine norovirus Newbury2 expected to prevent cross-species transmission. PLoS Pathog 5, e1000504