Both α2,3- and α2,6-Linked Sialic Acids on O-Linked Glycoproteins Act as Functional Receptors for Porcine Sapovirus

PLoS Pathogens

Volumn 10, Issue 6, 2014, Pages

  Kim, Deok Song ^a   Hosmillo, Myra ^a   Alfajaro, Mia Madel ^a   Kim, Ji Yun ^a   Park, Jun Gyu ^a   Son, Kyu Yeol ^a   Ryu, Eun Hye ^a   Sorgeloos, Frederic ^b   Kwon, Hyung Jun ^c   Park, Su Jin ^c   Lee, Woo Song ^c   Cho, Duck ^d   Kwon, Joseph ^e   Choi, Jong Soon ^e   Kang, Mun Il ^a   Goodfellow, Ian ^b   Cho, Kyoung Oh ^a  

^a Chonnam National University   (South Korea)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^d Chonnam National University Hwasun Hospital and Medical School   (South Korea)

^e Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD GROUP ANTIGEN; GLYCOPROTEIN; LECTIN; SIALIC ACID; SIALIDASE; VIRUS RECEPTOR; ENZYME INHIBITOR; LIGAND; MEMBRANE PROTEIN; SIALIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE ANALYSIS; CELL CULTURE; CONTROLLED STUDY; GASTROENTERITIS; GLYCOSYLATION; HEMAGGLUTINATION; HEMAGGLUTINATION TEST; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; ISOTOPE LABELING; MOLECULAR CLONING; NONHUMAN; NOROVIRUS; PIGLET; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SAPOVIRUS; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS PLAQUE; VIRUS STRAIN; ANIMAL; ANTAGONISTS AND INHIBITORS; CALICIVIRUS INFECTION; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; HOST PATHOGEN INTERACTION; INTESTINE MUCOSA; METABOLISM; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PIG; PROTEIN STABILITY; STEREOISOMERISM; SWINE DISEASE; VETERINARY; VIROLOGY;

ANIMALS; CALICIVIRIDAE INFECTIONS; CELL LINE; ENZYME INHIBITORS; GASTROENTERITIS; GLYCOSYLATION; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINAL MUCOSA; LIGANDS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; PROTEIN STABILITY; RECEPTORS, VIRUS; SAPOVIRUS; SIALIC ACIDS; STEREOISOMERISM; SUS SCROFA; SWINE; SWINE DISEASES;

EID: 84903445659     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004172     Document Type: Article

References (50)

1. Green KY (2007) Caliciviridae: The Noroviruses. In: Knipe DM, Howley PM, eds. Fields Virology, 5th edition. Philadelphia: Lippincott Willisams and Wilkins.
2. Nyström K, Le Gall-Reculé G, Grassi P, Abrantes J, Ruvoën-Clouet N, et al. (2011) Histo-blood group antigens act as attachment factors of rabbit hemorrhagic disease virus infection in a virus strain-dependent manner. PLoS Pathog 7: e1002188.
3. Radford AD, Coyne KP, Dawson S, Porter CJ, Gaskell RM, (2007) Feline calicivirus. Vet Res 38: 319-335.
4. Stuart AD, Brown TD, (2007) Alpha2,6-linked sialic acid acts as a receptor for Feline calicivirus. J Gen Virol 88: 177-186.
5. Tan M, Jiang X, (2010) Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog 6: e1000983.
6. Chang KO, Sosnovtsev SV, Belliot G, Kim Y, Saif LJ, et al. (2004) Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc Natl Acad Sci USA 101: 8733-8738.
7. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, et al. (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14: 1224-1231.
8. Hansman GS, Oka T, Katayama K, Takeda N, (2007) Human sapoviruses: genetic diversity, recombination, and classification. Re Med Virol 17: 133-141.
9. Ruvoen-Clouet N, Ganiere JP, Andre-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.
10. Zakhour M, Ruvoen-Clouet N, Charpilienne A, Langpap B, Poncet D, et al. (2009) The alphaGal 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.
11. Taube S, Perry JW, Yetming K, Patel SP, Auble H, et al. (2009) Gangloside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J Virol 83: 4092-4101.
12. Farkas T, Cross RW, Hargitt E 3rd, Lerche NW, Morrow AL, et al. (2010) Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. J Virol 84: 8617-8625.
13. Makino A, Shimojima M, Miyazawa T, Kato K, Tohya Y, et al. (2006) Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J Virol 80: 4482-4490.
14. Shirato-Horikoshi H, Ogawa S, Wakita T, Takeda N, (2007) Hansman (2007) Binding activity of norovirus and sapovirus to histo-blood group antigens. Arch Virol 152: 457-461.
15. Bank-Wolf BR, König M, Thiel HJ, (2010) Zoonotic aspects of infections with noroviruses and sapoviruses. Vet Microbiol 140: 204-212.
16. Mesquita JR, Costantini VP, Cannon JL, Lin SC, Nascimento MS, et al. (2013) Presence of antibodies against genogroup VI norovirus in humans. Virol J 10: 176.
17. Widdowson M, Rockx B, Schepp R, van der Poel WHM, Vinje J, et al. (2005) Detection of serum antibodies to bovine norovirus in veterinarians and the general population in the Netherlands. J Med Virol 76: 119-128.
18. Mattison K, Shukla A, Cook A, Pollari F, Friendship R, et al. (2007) Human noroviruses in swine and cattle. Emerg Infect Dis 13: 1184-1188.
19. Souza M, Azevedo MS, Jung K, Cheetham S, Saif LJ, (2008) Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. J Virol 82: 1777-1786.
20. Helenius A (2007) Virus Entry and Uncoating. In: Knipe DM, Howley PM, eds. Fields Virology, 5th edition. Philadelphia: Lippincott Willams and Wilkins.
21. Woolhouse MEJ, (2002) Population biology of emerging and re-emerging pathogens. Trends Microbiol 10: S3-S7.
22. Martínez-Barragán J, Angel RM, (2001) Identification of a putative coreceptor on Vero cells that participates in dengue 4 virus infection. J Virol 75: 7818-7827.
23. Woodward MP, Young WW Jr, Bloodgood RA, (1985) Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. J Immunol Methods 78: 143-153.
24. Hafenstein S, Bowman VD, Chipman PR, Kelly CMB, Lin F, et al. (2007) Interactionof decay-accelerating factor with coxsakievirus B3. J Virol 81: 12927-12935.
25. Olofsson S, Bergström T, (2005) Glycoconjugateglycans as viral receptors. Ann Med 37: 154-172.
26. Huang P, Xia M, Tan M, Zhong W, Wei C, et al. (2012) Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J Virol 86: 4833-4843.
27. Tan M, Zhong W, Song D, Thornton S, Jiang X, (2004) E. coli-expressed recombinant norovirus capsid proteins maintain authentic antigenicity and receptor binding capability. J Med Virol 74: 641-649.
28. Hanagata G, Gasa S, Sako F, Makita A, (1990) Human blood group A and H glycolipids in porcine plasma. Evidence for acquisition of the erythrocyte antigens from plasma. FEBS Lett 261: 312-314.
29. Guo M, Hayes J, Cho KO, Parwani AV, Lucas LM, et al. (2001) Comparative pathogenesis of tissue culture-adapted and wild-type Cowden porcine enteric calicivirus (PEC) in gnotobiotic pigs and induction of diarrhea by intravenous inoculation of wild-type PEC. J Virol 75: 9239-9251.
30. Huang P, Farkas T, Marionneau S, Zhong W, Ruvoen-Clouet N, et al. (2003) Noroviruses bind to human ABO, lewis, and secretor histo-blood group antigens: Identification of 4 distinct strain-specific patterns. J Infect Dis 188: 19-31.
31. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD, (2004) Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci USA 101: 4620-4624.
32. Varki A, (2007) Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 446: 1023-1029.
33. Sinibaldi L, Goldoni P, Seganti L, Superti F, Tsiang H, Orsi N, (1985) Gangliosides in early interactions between vesicular stomatitis virus and CER cells. Microbiologica 8: 355-365.
34. Taube S, Perry JW, McGreevy E, Yetming K, Perkins C, et al. (2012) Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. J Virol 86: 5584-5593.
35. Horzinek MC, (1973) Comparative aspects of togaviruses. J Gen Virol 20: 87-103.
36. McLeod GM, Wiggins HS, (1968) Bile-salts in small intestinal contents after ileal resection and in other malabsorption syndromes. Lancet 1: 873-876.
37. Ohtsubo K, Marth JD, (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126: 855-867.
38. Lopez S, Arias CF, (2006) Early steps in rotavirus cell entry. Curr Top Microbiol Immunol 309: 39-66.
39. Bhella D, Gatherer D, Chaudhry Y, Pink R, Goodfellow IG, (2008) Structural insights into calicivirus attachment and uncoating. J Virol 82(16): 8051-8058.
40. Ossiboff RJ, Zhou Y, Lightfoot PJ, Prasad BV, Parker JS, (2010) Conformational changes in the capsid of a calicivirus upon interaction with its functional receptor. J Virol 84(11): 5550-5564.
41. Bhella D, Goodfellow IG, (2011) The cryo-electron microscopy structure of feline calicivirus bound to junctional adhesion molecule A at 9-angstrom resolution reveals receptor-induced flexibility and two distinct conformational changes in the capsid protein VP1. J Virol 85(21): 11381-11390.
42. Walters RW, Yi SM, Keshavjee S, Brown KE, Welsh MJ, et al. (2001) Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer. J Biol Chem 276: 20610-20616.
43. Genzel Y, Dietzsch C, Rapp E, Schwarzer J, Reichl U, (2010) MDCK and Vero cells for influenza virus vaccine production: a one-to-one comparison up to lab-scale bioreactor cultivation. Appl Microbiol Biotechnol 88: 461-475.
44. Park SH, Saif LJ, Jeong C, Lim GK, Park SI, et al. (2006) Molecular characterization of novel G5 bovine rotavirus strains. J Clin Microbiol 44: 4101-4112.
45. Li X, Shou W, Xing X, Huang L, Tian L, et al. (2013) Overexpression of 4EBP1, p70S6K, Akt1 or Akt2 differentially promotes Coxsackievirus B3-induced apoptosis in HeLa cells. Cell Death Dis 4: e803-809.
46. Ryu MS, Jung EH, Cho KO, Kang SY, (2012) Expression of porcine sapovirus VP1 gene and VP1 specific monoclonal antibody production. Hybridoma 31: 155-162.
47. Huang P, Farkas T, Marionneau S, Zhong W, Ruvoen-Clouet N, et al. (2003) Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J Infect Dis 188: 19-31.
48. Huang P, Farkas T, Zhong W, Tan M, Thornton S, et al. (2005) Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns. J Virol 79: 6714-6722.
49. Fukushima K, Takahashi T, Takaguchi M, Ueyama H, Ito S, et al. (2011) Plaque formation assay for human parainfluenza virus type 1. Biol Pharm Bull 34: 996-1000.
50. Matrosovich M, Matrosovich T, Garten W, Klenk HD, (2006) New low-viscosity overlay medium for viral plaque assays. Virol J 3: 63.