Chemoenzymatic synthesis, characterization, and application of glycopolymers carrying lactosamine repeats as entry inhibitors against influenza virus infection

Glycobiology

Volumn 18, Issue 10, 2008, Pages 779-788

  Hidari, Kazuya I P J ^a   Murata, Takeomi ^b   Yoshida, Kazuhiro ^a   Takahashi, Yoshiharu ^b   Minamijima, Yo Hei ^a   Miwa, Yoshinobu ^c   Adachi, Satoshi ^c   Ogata, Makoto ^b   Usui, Taiichi ^b   Suzuki, Yasuo ^d   Suzuki, Takashi ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b SHIZUOKA UNIVERSITY   (Japan)

^c SHIZUOKA INSTITUTE OF ENVIRONMENT AND HYGIENE   (Japan)

^d CHUBU UNIVERSITY   (Japan)

Author keywords

Chemoenzymatic synthesis; Entry inhibitor; Glycopolymer; Influenza virus; Lactosamine repeat

Indexed keywords

ANTIVIRUS AGENT; GLYCOCONJUGATE; SIALYL N ACETYLLACTOSAMINE 2-6 ALPHA POLYGLUTAMIC ACID GLYCOPLYMER; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CELL STRAIN; CHEMOENZYMATIC SYNTHESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; DRUG SYNTHESIS; HEMAGGLUTINATION INHIBITION; HUMAN; INFLUENZA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SEQUENCE ANALYSIS; SWINE INFLUENZA VIRUS; TANDEM REPEAT; VIRAL RESPIRATORY TRACT INFECTION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS STRAIN;

AMINO SUGARS; ANIMALS; ANTIVIRAL AGENTS; BIOPOLYMERS; CARBOHYDRATE METABOLISM; CARBOHYDRATES; CELL LINE; DOGS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA, HUMAN; MICE; MODELS, MOLECULAR; MOLECULAR STRUCTURE; VIRUS INTERNALIZATION;

AVES; EQUIDAE; ORTHOMYXOVIRIDAE; SUIDAE;

EID: 51849164204     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwn067     Document Type: Article

References (47)

1. Chandrasekaran A, Srinivasan A, Raman R, Viswanathan K, Raguram S, Tumpey TM, Sasisekharan V, Sasisekharan R. 2008. Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat Biotechnol. 26:107-113.
2. Class EC, Osterhaus AD, van Beek R, De Jong JC, Rimmelzwaan GF, Senne DA, Krauss S, Shortridge KF, Webster RG. 1998. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351:472-477.
3. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol. 79:2814-2822.
4. Gambaryan A, Yamnikova S, Lvov D, Tuzikov A. Chinarev A, Pazynina G, Webster R, Matrosovich M, Bovin N. 2005. Receptor specificity of influenza viruses from birds and mammals: New data on involvement of the inner fragments of the carbohydrate chain. Virology. 334:276-283.
5. Gambaryan AS, Boravleva EY, Matrosovich TY, Matrosovich MN, Klenk H-D, Moiseeva EV, Tuzikov AB, Chinarev AA, Pazynina GV, Bovin NV. 2005. Polymer-bound 6′ sialyl-N-acetyllactosamine protects mice infected by influenza virus. Antiviral Res. 68:116-123.
6. Ha Y, Stevens DJ, Skehel JJ, Wiley DC. 2001. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci USA. 98:11181-11186.
7. Ha Y, Stevens DJ, Skehel JJ, Wiley DC. 2002. H5 avian and H9 swine influenza virus haemagglutinin structures: Possible origin of influenza subtypes. EMBO J. 21:865-875.
8. Hidari KIPJ, Shimada S, Suzuki Y, Suzuki T. 2007. Binding kinetics of influenza viruses to sialic acid-containing carbohydrates. Glycoconjugale J. 24:583-590.
9. Horimoto T, Kawaoka Y. 2005. Influenza: Lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol. 3:591-600.
10. Humphrey W, Dalke A, Schulten K. 1996. VMD: Visual molecular dynamics. J Mol Graph. 14:33-38.
11. Ito T, Suzuki Y, Mitnaul L, Vines A, Kida H, Kawaoka Y. 1997. Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology. 227:493-499.
12. Jones JC, Turpin EA, Bultmann H, Brandt CR, Schultz-Cherry S. 2006. Inhibition of influenza virus infection by a novel antiviral peptide that targets viral attachment to cells. J Virol. 80:11960-11967.
13. Kaplan EL, Meier P. 1958. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 53:457-481.
14. Kato T, Murata T, Usui T, Park EY. 2003. Improvement of GFPuv-β3GnT2 fusion protein production by suppressing protease in baculovirus expression system. Biosci Biotechnol Biochem. 67:2388-2395.
15. Kawaoka Y, Krauss S, Webster RG. 1989. Avian-to-human transmission of the PB1 Vne of influenza A viruses in the 1957 and 1968 pandemics. J Virol. 63:4603-4608.
16. Lees WJ, Spaltenstein A, Kingery-Wood JE, Whitesides GM. 1994. Polyacrylanudes bearing pendant alpha-sialoside groups strongly inhibit agglutination of erythrocytes by influenza A virus: Multivalency and steric stabilization of particulate biological systems. J Med Chem 37:3419-3433.
17. Lin YP, Shaw M, Gregory V, Cameron K, Lim W, Klimov A, Subbarao K, Guan Y, Krauss S, Shortridge K, et al. 2000. Avian-to-human transmission of H9N2 subtype influenza A viruses: Relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci USA. 97:9654-9658.
18. Lipatov AS, Govorkova EA, Webby RJ, Ozaki H, Peiris M, Guan Y, Poon L, Webster RG. 2004. Influenza: Emergence and control. J Virol. 78:8951-8959.
19. Makimura, Y, Watanabe S, Suzuki T, Suzuki Y, Ishida H, Kiso M, Katayama T, Kumagai H, Yamamoto K. 2006. Chemoenzymatic synthesis and application of a sialoglycopolymer with a chitosan backbone as a potent inhibitor of human influenza virus hemagglutination. Carbohydr Res. 341:1803-1808.
20. 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.
21. Miller-Podraza H, Johansson L, Johansson P, Larsson T, Matrosovich M, Karlsson K-A. 2000. A strain of human influenza A virus binds to extended but not short gangliosides as assayed by thin-layer chromatography overlay. Glycobiology. 10:975-982.
22. Murata T, Hattori T, Amarume S, Koichi A, Usui T. 2003. Kinetic studies on endo-β-galactosidase by a novel colorimetric assay and synthesis of N-acetyllactosamine-repeating oligosacchande β-glycosides using its transglycosylation activity. Eur J Biochem. 270:3709-3719.
23. Palese P. 2004. Influenza: Old and new threats. Nat Med. 10:S82-S87.
24. Peto R, Pike MC, Armitage P, Breslow NE, Cox DR, Howard SV, Mantel N, McPherson K, Peto J, Smith PG. 1977. Design and analysis of randomized clinical trials requiring prolonged observation of each patient: II. Analysis and examples. Br J Cancer. 35:1-39.
25. Reuter JD, Myc A, Hayes MM, Gan Z, Roy R, Qin D, Yin R, Piehler LT, Esfand R, Tomalia DA, et al. 1999. Inhibition of viral adhesion and infection by sialic-acid-conjugated dendritic polymers. Bioconjugate Chem. 10:271-278.
26. Sauter NK, Glick GD, Crowther RL, Park S-J, Eisen MB, Skehel JJ, Knowles JR, Wiley DC. 1992. Crystallographic detection of a second ligand binding site in influenza virus hemagglutinin. Proc Natl Acad Sci USA 89:324-328.
27. Scholtissek C, Rohde W, Von Hoyningen V, Rott R. 1978. On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology. 87:13-20.
28. Schwede T, Kopp J, Guex N, Peitsch MC. 2003. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
29. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y. 2006. Avian flu: Influenza virus receptors in the human airway. Nature. 440:435-436.
30. Sidwell RW, Huffman JH, Barnard DL, Bailey KW, Wong MEL Morrison A, Syndergaard T, Kim CU. 1998. Inhibition of influenza virus infections in mice by GS4104. an orally effective influenza virus neuraminidase inhibitor. Antiviral Res. 37:107-120.
31. Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA. 2006. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol. 355:1143-1155.
32. Stevens J, Blixt O, Paulson JC,Wilson IA. 2006b. Glycan microarray technologies: Tools to survey host specificity of influenza viruses. Nat Rev Microbiol. 4:857-864.
33. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. 2006. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science. 312:404-410.
34. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science. 303:1866-1870.
35. Suzuki Y. 2005. Sialobiology of influenza: Molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull. 28:399-408.
36. Suzuki Y, Matsunaga M, Matsumoto M. 1985. N-Acetylneuraminyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. Binding specificity of influenza virus A/Aichi/2/68 (H3N2) to membrane-associated GM3 with different molecular species of sialic acid. J Biol Chem. 260:1362-1365.
37. Suzuki Y, Nagao Y, Kato H, Matsumoto M, Nerome K, Nakajima K, Nobusawa E. 1986. Human influenza A virus hemagglutinin distinguishes sialyloligosaccharides in membrane-associated gangliosides as its receptor which mediates the adsorption and fusion processes of virus infection. Specificity for oligosaccharides and sialic acids and the sequence to which sialic acid is attached. J Biol Chem. 261:17057-17061.
38. Suzuki Y, Suzuki T, Matsumoto M. 1983. Isolation and characterization of receptor sialoglycoprotein for hemagglutinating virus of Japan (Sendai virus) from bovine erythrocyte membrane. J Biochem (Tokyo). 93:1621-1633.
39. Thompson CI, Barclay WS, Zambon MC, Pickles RJ. 2006. Infection of human airway epithelium by human and avian strains of influenza A virus. J Virol. 80:8060-8068.
40. Totani K, Kubota T, Kuroda T, Murata T, Hidari KIPJ, Suzuki T, Suzuki Y, Kobayashi K, Ashida H, Yamamoto K, et al. 2003. Chemoenzymatic synthesis and application of glycopolymers containing multivalent sialyloligosaccharides with a poly(L-glutamic acid) backbone for inhibition of infection by influenza viruses. Glycobiology. 13:315-326.
41. Usui T, Kubota S, Ohi H. 1993. A convenient synthesis of β-D-galactosyl disaccharide derivatives using the β-D-galactosidase from Bacillus circulans. Carbohydr Res. 244:315-323.
42. von Itzstein M, Wu WY, Kok GB, Pegg MS, Dyason JC, Jin B, Van Phan T, Smythe ML, White HF, Oliver SW, et al. 1993. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature. 363:418-423.
43. Watanabe W, Sudo K, Asawa S, Konno K, Yokota T, Shigeta S. 1995. Use of lactate dehydrogenase to evaluate the anti-viral activity against influenza A virus. J Virol Methods. 51:185-191.
44. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol Rev. 56:152-179.
45. Wright PF, Webster RG. 2001. Field Virology 4th ed. Philadelphia: Lippincott-Raven.
46. Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, Sakai-Tagawa Y, Muramoto Y, Ito M, Kiso M, Horimoto T, et al. 2006. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature. 444:378-382.
47. Zeng X, Nakaaki Y, Murata T, Usui T. 2000. Chemoenzymatic synthesis of glycopolypeptides carrying α-Neu5Ac-(2-3)-β-D-Gal-(1-3 -α-D-GalNAc, β-DGal- (1-3)-α-D-GalNAc, and related compounds and analysis of their specific interactions with lectins. Arch Biochem Biophys. 383:28-37.