Terminal sialic acid linkages determine different cell infectivities of human parainfluenza virus type 1 and type 3

Virology

Volumn 464-465, Issue 1, 2014, Pages 424-431

  Fukushima, Keijo ^a   Takahashi, Tadanobu ^a   Ito, Seigo ^a   Takaguchi, Masahiro ^a   Takano, Maiko ^a   Kurebayashi, Yuuki ^a   Oishi, Kenta ^a   Minami, Akira ^a   Kato, Tatsuya ^b   Park, Enoch Y ^b   Nishimura, Hidekazu ^c   Takimoto, Toru ^d   Suzuki, Takashi ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b SHIZUOKA UNIVERSITY   (Japan)

^c SENDAI CITY MEDICAL CENTER   (Japan)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

HPIV1; HPIV3; Human parainfluenza virus; Receptor specificity; Sialic acid; Sialic acid linkages

Indexed keywords

CELL RECEPTOR; GANGLIOSIDE; GLYCOPROTEIN; SIALIC ACID; SIALYLTRANSFERASE; N ACETYLNEURAMINIC ACID; PROTEIN BINDING; VIRUS RECEPTOR;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME SPECIFICITY; ERYTHROCYTE; NONHUMAN; PARAINFLUENZA VIRUS 1; PARAINFLUENZA VIRUS 3; PARAINFLUENZA VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ISOLATION; CELL LINE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PATHOGENICITY; RESPIROVIRUS INFECTION; VIROLOGY; VIRULENCE;

CELL LINE; HUMANS; N-ACETYLNEURAMINIC ACID; PARAINFLUENZA VIRUS 1, HUMAN; PARAINFLUENZA VIRUS 3, HUMAN; PROTEIN BINDING; RECEPTORS, VIRUS; RESPIROVIRUS INFECTIONS; VIRULENCE;

EID: 84919776201     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.07.033     Document Type: Article

References (40)

1. Aminoff D., Anderson J., Dabich L., Gathmann W.D. Sialic acid content of erythrocytes in normal individuals and patients with certain hematologic disorders. Am. J. Hematol. 1980, 9:381-389.
2. Amonsen M., Smith D.F., Cummings R.D., Air G.M. Human parainfluenza viruses hPIV1 and hPIV3 bind oligosaccharides with α2-3-linked sialic acids that are distinct from those bound by H5 avian influenza virus hemagglutinin. J. Virol. 2007, 81:8341-8345.
3. Baum L.G., Paulson J.C. Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem. Suppl. 1990, 40:35-38.
4. Bratosin D., Mazurier J., Debray H., Lecocq M., Boilly B., Alonso C., Moisei M., Motas C., Montreuil J. Flow cytofluorimetric analysis of young and senescent human erythrocytes probed with lectins. Evidence that sialic acids control their life span. Glycoconj. J. 1995, 12:258-267.
5. Bulai T., Bratosin D., Pons A., Montreuil J., Zanetta J.P. Diversity of the human erythrocyte membrane sialic acids in relation with blood groups. FEBS Lett. 2003, 534:185-189.
6. Chanock R. Parainfluenza viruses. Clin. Microbiol. Rev. 2001, 16:242-264.
7. Chu F.-L., Wen H.-L., Hou G.-H., Lin B., Zhang W.-Q., Song Y.-Y., Ren G.-J., Sun C.-X., Li Z.-M., Wang Z. Role of N-linked glycosylation of the human parainfluenza virus type 3 hemagglutinin-neuraminidase protein. Virus Res. 2013, 174:137-147.
8. Conyers S.M., Kidwell D.A. Chromogenic substrates for horseradish peroxidase. Anal. Biochem. 1991, 192:207-211.
9. Hoyer L.L., Roggentin P., Schauer R., Vimr E.R. Purification and properties of cloned Salmonella typhimurium LT2 sialidase with virus-typical kinetic preference for sialyl alpha 2→3 linkages. J. Biochem. 1991, 110:462-467.
10. Inaba N., Hiruma T., Togayachi A., Iwasaki H., Wang X.-H., Furukawa Y., Sumi R., Kudo T., Fujimura K., Iwai T., Gotoh M., Nakamura M., Narimatsu H. A novel I-branching β-1,6-N-acetylglucosaminyltransferase involved in human blood group I antigen expression. Blood 2003, 101:2870-2876.
11. Kaludov N., Brown K.E., Walters R.W., Zabner J., Chiorini J.A. Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J. Virol. 2001, 75:6884-6893.
12. Kirsch S., Müthing J., Peter-Katalinić J., Bindila L. On-line nano-HPLC/ESI QTOF MS monitoring of α2-3 and α2-6 sialylation in granulocyte glycosphingolipidome. Biol. Chem. 2009, 390:657-672.
13. Lee Y.C., Kojima N., Wada E., Kurosawa N., Nakaoka T., Hamamoto T., Tsuji S. Cloning and expression of cDNA for a new type of Galβ1,3GalNAc alpha 2,3-sialyltransferase. J. Biol. Chem. 1994, 269:10028-10033.
14. Loveless R.W., Feizi T. Sialo-oligosaccharide receptors for Mycoplasma pneumoniae and related oligosaccharides of poly-N-acetyllactosamine series are polarized at the cilia and apical-microvillar domains of the ciliated cells in human bronchial epithelium. Infect. Immun. 1989, 57:1285-1289.
15. Markwell M.A., Paulson J.C. Sendai virus utilizes specific sialyloligosaccharides as host cell receptor determinants. Proc. Natl. Acad. Sci. USA 1980, 77:5693-5697.
16. Markwell M.A., Svennerholm L., Paulson J.C. Specific gangliosides function as host cell receptors for Sendai virus. Proc. Natl. Acad. Sci. USA 1981, 78:5406-5410.
17. Matrosovich M.N., Gambaryan A.S., Teneberg S., Piskarev V.E., Yamnikova S.S., Lvov D.K., Robertson J.S., Karlsson K.A. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 1997, 233:224-234.
18. Ogata M., Nakajima M., Kato T., Obara T., Yagi H., Kato K., Usui T., Park E.Y. Synthesis of sialoglycopolypeptide for potentially blocking influenza virus infection using a rat α2,6-sialyltransferase expressed in BmNPV bacmid-injected silkworm larvae. BMC Biotechnol. 2009, 9:54.
19. Rillahan C.D., Antonopoulos A., Lefort C.T., Sonon R., Azadi P., Ley K., Dell A., Haslam S.M., Paulson J.C. Global metabolic inhibitors of sialyl- and fucosyltransferases remodel the glycome. Nat. Chem. Biol. 2012, 8:661-668.
20. Rogerieux F., Belaise M., Terzidis-Trabelsi H., Greffard A., Pilatte Y., Lambré C.R. Determination of the sialic acid linkage specificity of sialidases using lectins in a solid phase assay. Anal. Biochem. 1993, 211:200-204.
21. Sánchez-Felipe L., Villar E., Muñoz-Barroso I. α2-3- and α2-6- N-linked sialic acids allow efficient interaction of Newcastle Disease Virus with target cells. Glycoconj. J. 2012, 29:539-549.
22. Scheid A., Caliguiri L.A., Compans R.W., Choppin P.W. Isolation of paramyxovirus glycoproteins. Association of both hemagglutinating and neuraminidase activities with the larger SV5 glycoprotein. Virology 1972, 50:640-652.
23. Sinaniotis C. Viral pneumoniae in children: incidence and aetiology. Paediatr. Respir. Rev. 2004, 5:S197-S200.
24. Song X., Yu H., Chen X., Lasanajak Y., Tappert M.M., Air G.M., Tiwari V.K., Cao H., Chokhawala H.a., Zheng H., Cummings R.D., Smith D.F. A sialylated glycan microarray reveals novel interactions of modified sialic acids with proteins and viruses. J. Biol. Chem. 2011, 286:31610-31622.
25. Suzuki T., Ikeda K., Koyama N., Hosokawa C., Kogure T., Takahashi T., Jwa Hidari K.I., Miyamoto D., Tanaka K., Suzuki Y. Inhibition of human parainfluenza virus type 1 sialidase by analogs of 2-deoxy-2,3-didehydro-N-acetylneuraminic acid. Glycoconj. J. 2001, 18:331-337.
26. Suzuki T., Portner A., Scroggs R.A., Uchikawa M., Koyama N., Matsuo K., Suzuki Y., Takimoto T. Receptor specificities of human respiroviruses. J. Virol. 2001, 75:4604-4613.
27. Suzuki Y. Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol. Pharm. Bull. 2005, 28:399-408.
28. Suzuki Y., Ito T., Suzuki T., Holland R.E., Chambers T.M., Kiso M., Ishida H., Kawaoka Y. Sialic acid species as a determinant of the host range of influenza A viruses. J. Virol. 2000, 74:11825-11831.
29. Suzuki Y., Suzuki T., Matsunaga M., Matsumoto M. Gangliosides as paramyxovirus receptor. Structural requirement of sialo-oligosaccharides in receptors for hemagglutinating virus of Japan (Sendai virus) and Newcastle disease virus. J. Biochem. 1985, 97:1189-1199.
30. Takaguchi M., Takahashi T., Hosokawa C., Ueyama H., Fukushima K., Hayakawa T., Itoh K., Ikeda K., Suzuki T. A single amino acid mutation at position 170 of human parainfluenza virus type 1 fusion glycoprotein induces obvious syncytium formation and caspase-3-dependent cell death. J. Biochem. 2011, 149:191-202.
31. Takahashi T., Ito K., Fukushima K., Takaguchi M., Hayakawa T., Suzuki Y., Suzuki T. Sulfatide negatively regulates the fusion process of human parainfluenza virus type 3. J. Biochem. 2012, 152:373-380.
32. Takahashi T., Murakami K., Nagakura M., Kishita H., Watanabe S., Honke K., Ogura K., Tai T., Kawasaki K., Miyamoto D., Hidari K.I.P.J., Guo C.-T., Suzuki Y., Suzuki T. Sulfatide is required for efficient replication of influenza A virus. J. Virol. 2008, 82:5940-5950.
33. Tozawa H., Watanabe M., Ishida N. Structural components of Sendai virus. Serological and physicochemical characterization of hemagglutinin subunit associated with neuraminidase activity. Virology 1973, 55:242-253.
34. Tsukamoto H., Takakura Y., Yamamoto T. Purification, cloning, and expression of an α/β-galactoside α-2,3-sialyltransferase from a luminous marine bacterium, Photobacterium phosphoreum. J. Biol. Chem. 2007, 282:29794-29802.
35. Uchida Y., Tsukada Y., Sugimori T. Enzymatic properties of neuraminidases from Arthrobacter ureafaciens. J. Biochem. 1979, 86:1573-1585.
36. Vierbuchen M., Uhlenbruck G., Ortmann M., Dufhues G., Fischer R. Occurrence and distribution of glycoconjugates in human tissues as detected by the Erythrina cristagalli lectin. J. Histochem. Cytochem. 1988, 36:367-376.
37. Williams M.A., Kitagawa H., Datta A.K., Paulson J.C., Jamieson J.C. Large-scale expression of recombinant sialyltransferases and comparison of their kinetic properties with native enzymes. Glycoconj. J. 1995, 12:755-761.
38. Yamamoto T., Nakashizuka M., Kodama H., Kajihara Y., Terada I. Purification and characterization of a marine bacterial β-galactoside α2,6-sialyltransferase from Photobacterium damsela JT0160. J. Biochem. 1996, 120:104-110.
39. Yamamoto T., Nakashizuka M., Terada I. Cloning and expression of a marine bacterial β-galactoside α2,6-sialyltransferase gene from Photobacterium damsela JT0160. J. Biochem. 1998, 123:94-100.
40. Zhang L., Bukreyev A., Thompson C.I., Watson B., Peeples M.E., Collins P.L., Pickles R.J. Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. Society 2005, 79:1113-1124.