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

Journal of General Virology

Volumn 92, Issue 6, 2011, Pages 1398-1409

  Mauroy, Axel ^a   Gillet, Laurent ^a   Mathijs, Elisabeth ^a   Vanderplasschen, Alain ^a   Thiry, Etienne ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSIDASE; AMILORIDE; CHLOROQUINE; CHLORPROMAZINE; CHONDROITIN SULFATE; CYTOCHALASIN D; HEPARAN SULFATE; NYSTATIN; PHOSPHOLIPASE C; TRYPSIN;

ANIMAL CELL; ARTICLE; CATTLE; ENDOCYTOSIS; FLOW CYTOMETRY; GENOTYPE; INTERNALIZATION; KIDNEY CELL; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STRAIN IDENTIFICATION; VIRUS CELL INTERACTION; VIRUS LIKE AGENT;

ANIMALS; CALICIVIRIDAE INFECTIONS; CATTLE; CATTLE DISEASES; CELL LINE; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; NOROVIRUS; PHYLOGENY; PROTEIN BINDING; SPODOPTERA; VIRAL PROTEINS; VIRUS INTERNALIZATION;

BOVINAE; CALICIVIRIDAE; NOROVIRUS;

EID: 79956316171     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.030072-0     Document Type: Article

References (51)

1. Baranowski, E., Ruiz-Jarabo, C. M. & Domingo, E. (2001). Evolution of cell recognition by viruses. Science 292, 1102-1105.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. Girao, H., Geli, M. I. & Idrissi, F. Z. (2008). Actin in the endocytic pathway: from yeast to mammals. FEBS Lett 582, 2112-2119.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. Marsh, M. & Helenius, A. (2006). Virus entry: open sesame. Cell 124, 729-740.
21. 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.
22. 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.
23. 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.
24. Miller, N. & Hutt-Fletcher, L. M. (1992). Epstein-Barr virus enters B cells and epithelial cells by different routes. J Virol 66, 3409-3414.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. Scipioni, A., Mauroy, A., Vinjé, J. & Thiry, E. (2008). Animal noroviruses. Vet J 178, 32-45.
37. Sieczkarski, S. B. & Whittaker, G. R. (2002). Dissecting virus entry via endocytosis. J Gen Virol 83, 1535-1545.
38. Smith, A. E. & Helenius, A. (2004). How viruses enter animal cells. Science 304, 237-242.
39. 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.
40. 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.
41. 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.
42. Tan, M. & Jiang, X. (2005). Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol 13, 285-293.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. Yanagi, Y., Takeda, M., Ohno, S. & Hashiguchi, T. (2009). Measles virus receptors. Curr Top Microbiol Immunol 329, 13-30.
51. 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