The use of sialidase therapy for respiratory viral infections

Antiviral Research

Volumn 98, Issue 3, 2013, Pages 401-409

  Nicholls, John M ^a   Moss, Ronald B ^b   Haslam, Stuart M ^c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b Ansun BioPharma   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Antiviral therapy; Influenza; Sialic acid; Sialidase

Indexed keywords

ANTIVIRUS AGENT; BACTERIAL ENZYME; DAS 181; EPITHELIAL CELL ADHESION MOLECULE; SIA ALPHA2; SIA ALPHA3; SIA ALPHA4; SIA ALPHA5; SIA ALPHA6; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIVIRAL ACTIVITY; CHEMICAL STRUCTURE; DRUG POTENCY; DRUG TOLERABILITY; ENZYME DEGRADATION; HUMAN; INFLUENZA A; INFLUENZA B; NONHUMAN; PARAINFLUENZA VIRUS; PARAINFLUENZA VIRUS INFECTION; PRIORITY JOURNAL; REVIEW; VIRUS CELL INTERACTION;

ACETYLATION; ANIMALS; ANTIVIRAL AGENTS; BACTERIAL PROTEINS; CLINICAL TRIALS AS TOPIC; GLYCOPROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PARAMYXOVIRIDAE; PARAMYXOVIRIDAE INFECTIONS; RECEPTORS, VIRUS; RECOMBINANT FUSION PROTEINS; RESPIRATORY TRACT INFECTIONS;

BACTERIA (MICROORGANISMS); SIA;

EID: 84877097783     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2013.04.012     Document Type: Review

References (101)

1. Air G.M., Laver W.G. Red cells bound to influenza virus N9 neuraminidase are not released by the N9 neuraminidase activity. Virology 1995, 211:278-284.
2. Al-qattan M.N., Mordi M.N. Docking of sialic acid analogues against influenza A hemagglutinin: a correlational study between experimentally measured and computationally estimated affinities. J. Mol. Model. 2010, 16:1047-1058.
3. Al-qattan M.N., Mordi M.N. Site-directed fragment-based generation of virtual sialic acid databases against influenza A hemagglutinin. J. Mol. Model. 2010, 16:975-991.
4. Argueso P., Sumiyoshi M. Characterization of a carbohydrate epitope defined by the monoclonal antibody H185: sialic acid O-acetylation on epithelial cell-surface mucins. Glycobiology 2006, 16:1219-1228.
5. Arming S., Wipfler D., Mayr J., Merling A., Vilas U., Schauer R., Schwartz-Albiez R., Vlasak R. The human Cas1 protein: a sialic acid-specific O-acetyltransferase?. Glycobiology 2011, 21:553-564.
6. Banks D.D. The effect of glycosylation on the folding kinetics of erythropoietin. J. Mol. Biol. 2011, 412:536-550.
7. Bergelson L.D., Bukrinskaya A.G., Prokazova N.V., Shaposhnikova G.I., Kocharov S.L., Shevchenko V.P., Kornilaeva G.V., Fomina-Ageeva E.V. Role of gangliosides in reception of influenza virus. Eur. J. Biochem. 1982, 128:467-474.
8. Biondi C., Cotorruelo C., Ensinck A., Garcia Borras S., Racca L., Racca A. Senescent erythrocytes: factors affecting the aging of red blood cells. Immunol. Invest. 2002, 31:41-50.
9. Blessia T.F., Rapheal V.S., Sharmila D.J. Molecular dynamics of sialic acid analogues and their interaction with influenza hemagglutinin. Indian J. Pharm. Sci. 2010, 72:449-457.
10. Blomqvist S., Savolainen C., Raman L., Roivainen M., Hovi T. Human rhinovirus 87 and enterovirus 68 represent a unique serotype with rhinovirus and enterovirus features. J. Clin. Microbiol. 2002, 40:4218-4223.
11. Bratosin D., Mazurier J., Tissier J.P., Estaquier J., Huart J.J., Ameisen J.C., Aminoff D., Montreuil J. Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. A review. Biochimie 1998, 80:173-195.
12. Brundage J.F., Shanks G.D. Deaths from bacterial pneumonia during 1918-19 influenza pandemic. Emerg. Infect. Dis. 2008, 14:1193-1199.
13. 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.
14. Busser B., Sancey L., Brambilla E., Coll J.L., Hurbin A. The multiple roles of amphiregulin in human cancer. Biochim. Biophys. Acta 2011, 1816:119-131.
15. Cao H., Li Y., Lau K., Muthana S., Yu H., Cheng J., Chokhawala H.A., Sugiarto G., Zhang L., Chen X. Sialidase substrate specificity studies using chemoenzymatically synthesized sialosides containing C5-modified sialic acids. Org. Biomol. Chem. 2009, 7:5137-5145.
16. Chan R.W., Chan M.C., Wong A.C., Karamanska R., Dell A., Haslam S.M., Sihoe A.D., Chui W.H., Triana-Baltzer G., Li Q., Peiris J.S., Fang F., Nicholls J.M. DAS181 inhibits H5N1 influenza virus infection of human lung tissues. Antimicrob. Agents Chemother. 2009, 53:3935-3941.
17. Chen X., Varki A. Advances in the biology and chemistry of sialic acids. ACS Chem. Biol. 2010, 5:163-176.
18. Chen Y.B., Driscoll J.P., McAfee S.L., Spitzer T.R., Rosenberg E.S., Sanders R., Moss R.B., Fang F., Marty F.M. Treatment of parainfluenza 3 infection with DAS181 in a patient after allogeneic stem cell transplantation. Clin. Infect. Dis. 2011, 53:e77-80.
19. Corfield A.P., Veh R.W., Wember M., Michalski J.C., Schauer R. The release of N-acetyl- and N-glycolloyl-neuraminic acid from soluble complex carbohydrates and erythrocytes by bacterial, viral and mammalian sialidases. Biochem. J. 1981, 197:293-299.
20. Corfield A.P., Higa H., Paulson J.C., Schauer R. The specificity of viral and bacterial sialidases for alpha(2-3)- and alpha(2-6)-linked sialic acids in glycoproteins. Biochim. Biophys. Acta 1983, 744:121-126.
21. Davies L.R., Pearce O.M., Tessier M.B., Assar S., Smutova V., Pajunen M., Sumida M., Sato C., Kitajima K., Finne J., Gagneux P., Pshezhetsky A., Woods R., Varki A. Metabolism of vertebrate amino sugars with N-glycolyl groups: resistance of alpha2-8-linked N-glycolylneuraminic acid to enzymatic cleavage. J. Biol. Chem. 2012, 287:28917-28931.
22. Drozd D.R., Limaye A.P., Moss R.B., Sanders R.L., Hansen C., Edelman J.D., Raghu G., Boeckh M., Rakita R.M. DAS181 treatment of severe parainfluenza type 3 pneumonia in a lung transplant recipient. Transpl. Infect. Dis. 2012, 15. E28-32.
23. Gottschalk A., De St Fezekas., Groth S. On the relationship between the indicator profile and prosthetic group of mucoproteins inhibitory for influenza virus haemagglutinin. J. Gen. Microbiol. 1960, 22:690-697.
24. Grewal P.K., Uchiyama S., Ditto D., Varki N., Le D.T., Nizet V., Marth J.D. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat. Med. 2008, 14:648-655.
25. Griffin J.A., Basak S., Compans R.W. Effects of hexose starvation and the role of sialic acid in influenza virus release. Virology 1983, 125:324-334.
26. Grijalva C.G., Griffin M.R. Unveiling the burden of influenza-associated pneumococcal pneumonia. J. Infect. Dis. 2012, 205:355-357.
27. Gut H., King S.J., Walsh M.A. Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase. FEBS Lett. 2008, 582:3348-3352.
28. Guzman-Suarez B.B., Buckley M.W., Gilmore E.T., Vocca E., Moss R., Marty F.M., Sanders R., Baden L.R., Wurtman D., Issa N.C., Fang F., Koo S. Clinical potential of DAS181 for treatment of parainfluenza-3 infections in transplant recipients. Transpl. Infect. Dis. 2012, 14:427-433.
29. Haffajee A.D., Cugini M.A., Dibart S., Smith C., Kent R.L., Socransky S.S. Clinical and microbiological features of subjects with adult periodontitis who responded poorly to scaling and root planing. J. Clin. Periodontol. 1997, 24:767-776.
30. Hanaoka K., Pritchett T.J., Takasaki S., Kochibe N., Sabesan S., Paulson J.C., Kobata A. 4-O-acetyl-N-acetylneuraminic acid in the N-linked carbohydrate structures of equine and guinea pig alpha 2-macroglobulins, potent inhibitors of influenza virus infection. J. Biol. Chem. 1989, 264:9842-9849.
31. Harduin-Lepers A., Mollicone R., Delannoy P., Oriol R. The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology 2005, 15:805-817.
32. Hedlund M., Aschenbrenner L.M., Jensen K., Larson J.L., Fang F. Sialidase-based anti-influenza virus therapy protects against secondary pneumococcal infection. J. Infect. Dis. 2010, 201:1007-1015.
33. Helander A., Silvey K.J., Mantis N.J., Hutchings A.B., Chandran K., Lucas W.T., Nibert M.L., Neutra M.R. The viral sigma1 protein and glycoconjugates containing alpha2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. J. Virol. 2003, 77:7964-7977.
34. Herfst S., Schrauwen E.J., Linster M., Chutinimitkul S., de Wit E., Munster V.J., Sorrell E.M., Bestebroer T.M., Burke D.F., Smith D.J., Rimmelzwaan G.F., Osterhaus A.D., Fouchier R.A. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012, 336:1534-1541.
35. Hildebrandt H., Muhlenhoff M., Gerardy-Schahn R. Polysialylation of NCAM. Adv Exp. Med. Biol. 2010, 663:95-109.
36. Imai M., Watanabe T., Hatta M., Das S.C., Ozawa M., Shinya K., Zhong G., Hanson A., Katsura H., Watanabe S., Li C., Kawakami E., Yamada S., Kiso M., Suzuki Y., Maher E.A., Neumann G., Kawaoka Y. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012, 486:420-428.
37. Iverson A.R., Boyd K.L., McAuley J.L., Plano L.R., Hart M.E., McCullers J.A. Influenza virus primes mice for pneumonia from Staphylococcus aureus. J. Infect. Dis. 2011, 203:880-888.
38. Karlstrom A., Heston S.M., Boyd K.L., Tuomanen E.I., McCullers J.A. Toll-like receptor 2 mediates fatal immunopathology in mice during treatment of secondary pneumococcal pneumonia following influenza. J. Infect. Dis. 2011, 204:1358-1366.
39. Kim S., Oh D.B., Kang H.A., Kwon O. Features and applications of bacterial sialidases. Appl. Microbiol. Biotechnol. 2011, 91:1-15.
40. Klein A., Roussel P. O-acetylation of sialic acids. Biochimie 1998, 80:49-57.
41. Larson J.L., Kang S.K., Choi B.I., Hedlund M., Aschenbrenner L.M., Cecil B., Machado G., Nieder M., Fang F. A safety evaluation of DAS181, a sialidase fusion protein, in rodents. Toxicol. Sci. 2011, 122:567-578.
42. Lehmann F., Tiralongo E., Tiralongo J. Sialic acid-specific lectins: occurrence, specificity and function. Cell Mol. Life Sci. 2006, 63:1331-1354.
43. Lentz T.L. Binding of viral attachment protein to host-cell receptor: the Achilles heel of infectious viruses. Trends Pharmacol. Sci. 1988, 9:247-252.
44. Lentz T.L. The recognition event between virus and host cell receptor: a target for antiviral agents. J. Gen. Virol. 1990, 71(Pt 4):751-766.
45. Li, X.B., Wang, S.Q., Xu, W.R., Wang, R.L., Chou, K.C., 2011. Novel inhibitor design for hemagglutinin against H1N1 influenza virus by core hopping method. PLoS One 6, e28111.
46. Mahanonda R., Seymour G.J., Powell L.W., Good M.F., Halliday J.W. Limit dilution analysis of peripheral blood T lymphocytes specific to periodontopathic bacteria. Clin. Exp. Immunol. 1989, 75:245-251.
47. Malakhov M.P., Aschenbrenner L.M., Smee D.F., Wandersee M.K., Sidwell R.W., Gubareva L.V., Mishin V.P., Hayden F.G., Kim D.H., Ing A., Campbell E.R., Yu M., Fang F. Sialidase fusion protein as a novel broad-spectrum inhibitor of influenza virus infection. Antimicrob. Agents Chemother. 2006, 50:1470-1479.
48. Manco S., Hernon F., Yesilkaya H., Paton J.C., Andrew P.W., Kadioglu A. Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect Immun 2006, 74:4014-4020.
49. Mandal C., Chatterjee M., Sinha D. Investigation of 9-O-acetylated sialoglycoconjugates in childhood acute lymphoblastic leukaemia. Br. J. Haematol. 2000, 110:801-812.
50. Martin L.T., Verhagen A., Varki A. Recombinant influenza C hemagglutinin-esterase as a probe for sialic acid 9-O-acetylation. Methods Enzymol. 2003, 363:489-498.
51. Matrosovich M.N., Matrosovich T.Y., Gray T., Roberts N.A., Klenk H.D. Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J. Virol. 2004, 78:12665-12667.
52. McCullers J.A., McAuley J.L., Browall S., Iverson A.R., Boyd K.L., Henriques Normark B. Influenza enhances susceptibility to natural acquisition of and disease due to Streptococcus pneumoniae in ferrets. J. Infect. Dis. 2010, 202:1287-1295.
53. Moscona A., Porotto M., Palmer S., Tai C., Aschenbrenner L., Triana-Baltzer G., Li Q.X., Wurtman D., Niewiesk S., Fang F. A recombinant sialidase fusion protein effectively inhibits human parainfluenza viral infection in vitro and in vivo. J. Infect. Dis. 2010, 202:234-241.
54. Moscona A. Entry of parainfluenza virus into cells as a target for interrupting childhood respiratory disease. J. Clin. Invest. 2005, 115:1688-1698.
55. Moss R.B., Hansen C., Sanders R.L., Hawley S., Li T., Steigbigel R.T. A Phase II study of DAS181, a novel host directed antiviral for the treatment of influenza infection. J. Infect. Dis. 2012, 206:1844-1851.
56. Nandi T. Proposed lead molecules against Hemagglutinin of avian influenza virus (H5N1). Bioinformation 2008, 2:240-244.
57. Nelson G.E., Gershman K.A., Swerdlow D.L., Beall B.W., Moore M.R. Invasive pneumococcal disease and pandemic (H1N1) 2009, Denver, Colorado, USA. Emerg. Infect. Dis. 2012, 18:208-216.
58. Newstead S.L., Potter J.A., Wilson J.C., Xu G., Chien C.H., Watts A.G., Withers S.G., Taylor G.L. The structure of Clostridium perfringens NanI sialidase and its catalytic intermediates. J. Biol. Chem. 2008, 283:9080-9088.
59. Nicholls J.M., Bourne A.J., Chen H., Guan Y., Peiris J.S. Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respir. Res. 2007, 8:73.
60. Nicholls J.M., Aschenbrenner L.M., Paulson J.C., Campbell E.R., Malakhov M.P., Wurtman D.F., Yu M., Fang F. Comment on: concerns of using sialidase fusion protein as an experimental drug to combat seasonal and pandemic influenza. J. Antimicrob. Chemother. 2008, 62:426-428. (author reply 428-429).
61. O'Neill A.S., van den Berg T.K., Mullen G.E. Sialoadhesin - A macrophage-restricted marker of immunoregulation and inflammation. Immunology 2013, 138:198-207.
62. Paulson J.C., Rademacher C. Glycan terminator. Nat. Struct. Mol. Biol. 2009, 16:1121-1122.
63. Paulson J.C., Sadler J.E., Hill R.L. Restoration of specific myxovirus receptors to asialoerythrocytes by incorporation of sialic acid with pure sialyltransferases. J. Biol. Chem. 1979, 254:2120-2124.
64. Pettigrew M.M., Fennie K.P., York M.P., Daniels J., Ghaffar F. Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types. Infect. Immun. 2006, 74:3360-3365.
65. Plotkowski M.C., Puchelle E., Beck G., Jacquot J., Hannoun C. Adherence of type I Streptococcus pneumoniae to tracheal epithelium of mice infected with influenza A/PR8 virus. Am. Rev. Respir. Dis. 1986, 134:1040-1044.
66. Plumbridge J., Vimr E. Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli. J. Bacteriol. 1999, 181:47-54.
67. Porotto M., Greengard O., Poltoratskaia N., Horga M.A., Moscona A. Human parainfluenza virus type 3 HN-receptor interaction: effect of 4-guanidino-Neu5Ac2en on a neuraminidase-deficient variant. J. Virol. 2001, 75:7481-7488.
68. Pritchett T.J., Paulson J.C. Basis for the potent inhibition of influenza virus infection by equine and guinea pig alpha 2-macroglobulin. J. Biol. Chem. 1989, 264:9850-9858.
69. Pritchett T.J., Brossmer R., Rose U., Paulson J.C. Recognition of monovalent sialosides by influenza virus H3 hemagglutinin. Virology 1987, 160:502-506.
70. Reyes-Leyva J., Banos R., Borraz-Arguello M., Santos-Lopez G., Rosas N., Alvarado G., Herrera I., Vallejo V., Tapia-Ramirez J. Amino acid change 335 E to K affects the sialic-acid-binding and neuraminidase activities of Urabe AM9 mumps virus hemagglutinin-neuraminidase glycoprotein. Microbes Infect. 2007, 9:234-240.
71. Rogers G.N., Paulson J.C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127:361-373.
72. Rogers G.N., Pritchett T.J., Lane J.L., Paulson J.C. Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants. Virology 1983, 131:394-408.
73. Schauer R., Srinivasan G.V., Wipfler D., Kniep B., Schwartz-Albiez R. O-Acetylated sialic acids and their role in immune defense. Adv. Exp. Med. Biol. 2011, 705:525-548.
74. Schauer R. Chemistry and biology of the acylneuraminic acids. Angew. Chem. Int. Ed. Engl. 1973, 12:127-138.
75. Schauer R. Achievements and challenges of sialic acid research. Glycoconj. J. 2000, 17:485-499.
76. Shoyab M., McDonald V.L., Bradley J.G., Todaro G.J. Amphiregulin: a bifunctional growth-modulating glycoprotein produced by the phorbol 12-myristate 13-acetate-treated human breast adenocarcinoma cell line MCF-7. Proc. Natl. Acad. Sci. USA 1988, 85:6528-6532.
77. 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.
78. Sorrell E.M., Wan H., Araya Y., Song H., Perez D.R. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc. Natl. Acad. Sci. USA 2009, 106:7565-7570.
79. Sosroseno W., Bird P.S., Gemmell E., Seymour G.J. The induction of oral tolerance to Actinomyces viscosus in mice. Oral Dis. 2006, 12:387-394.
80. Springer G.F., Ansell N.J. Inactivation of human erythrocyte agglutinogens M and N by influenza viruses and receptor-destroying enzyme. Proc. Natl. Acad. Sci. USA 1958, 44:182-189.
81. Stafford G., Roy S., Honma K., Sharma A. Sialic acid, periodontal pathogens and Tannerella forsythia: stick around and enjoy the feast!. Mol. Oral Microbiol. 2012, 27:11-22.
82. Sun S., Wang Q., Zhao F., Chen W., Li Z. Glycosylation site alteration in the evolution of influenza A (H1N1) viruses. PLoS One 2011, 6:e22844.
83. 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.
84. Taylor H.P., Cooper N.R. Human cytomegalovirus binding to fibroblasts is receptor mediated. J. Virol. 1989, 63:3991-3998.
85. Teufel M., Roggentin P., Schauer R. Properties of sialidase isolated from Actinomyces viscosus DSM 43798. Biol. Chem. Hoppe Seyler 1989, 370:435-443.
86. Thompson C.I., Barclay W.S., Zambon M.C., Pickles R.J. Infection of human airway epithelium by human and avian strains of influenza a virus. J. Virol. 2006, 80:8060-8068.
87. Triana-Baltzer G.B., Gubareva L.V., Nicholls J.M., Pearce M.B., Mishin V.P., Belser J.A., Chen L.M., Chan R.W., Chan M.C., Hedlund M., Larson J.L., Moss R.B., Katz J.M., Tumpey T.M., Fang F. Novel pandemic influenza A(H1N1) viruses are potently inhibited by DAS181, a sialidase fusion protein. PLoS One 2009, 4:e7788.
88. Triana-Baltzer G.B., Babizki M., Chan M.C., Wong A.C., Aschenbrenner L.M., Campbell E.R., Li Q.X., Chan R.W., Peiris J.S., Nicholls J.M., Fang F. DAS181, a sialidase fusion protein, protects human airway epithelium against influenza virus infection: an in vitro pharmacodynamic analysis. J. Antimicrob. Chemother. 2010, 65:275-284.
89. van der Sluijs K.F., van Elden L.J., Nijhuis M., Schuurman R., Florquin S., Shimizu T., Ishii S., Jansen H.M., Lutter R., van der Poll T. Involvement of the platelet-activating factor receptor in host defense against Streptococcus pneumoniae during postinfluenza pneumonia. Am. J. Physiol. Lung Cell Mol. Physiol. 2006, 290:L194-L199.
90. Varki A., Gagneux P. Multifarious roles of sialic acids in immunity. Ann. N. Y. Acad. Sci. 2012, 1253:16-36.
91. Varki N.M., Varki A. Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab. Invest. 2007, 87:851-857.
92. Varki A. Sialic acids as ligands in recognition phenomena. FASEB J. 1997, 11:248-255.
93. Villar E., Barroso I.M. Role of sialic acid-containing molecules in paramyxovirus entry into the host cell: a minireview. Glycoconj. J. 2006, 23:5-17.
94. Vimr E.R., Kalivoda K.A., Deszo E.L., Steenbergen S.M. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 2004, 68:132-153.
95. Vimr E.R. Microbial sialidases: does bigger always mean better?. Trends Microbiol. 1994, 2:271-277.
96. Weigl J.A., Puppe W., Meyer C.U., Berner R., Forster J., Schmitt H.J., Zepp F. Ten years' experience with year-round active surveillance of up to 19 respiratory pathogens in children. Eur. J. Pediatr. 2007, 166:957-966.
97. Weis W., Brown J.H., Cusack S., Paulson J.C., Skehel J.J., Wiley D.C. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 1988, 333:426-431.
98. Wilks S., de Graaf M., Smith D.J., Burke D.F. A review of influenza haemagglutinin receptor binding as it relates to pandemic properties. Vaccine 2012, 30:4369-4376.
99. Willmarth N.E., Baillo A., Dziubinski M.L., Wilson K., Riese D.J., Ethier S.P. Altered EGFR localization and degradation in human breast cancer cells with an amphiregulin/EGFR autocrine loop. Cell Signal. 2009, 21:212-219.
100. Xia B., Royall J.A., Damera G., Sachdev G.P., Cummings R.D. Altered O-glycosylation and sulfation of airway mucins associated with cystic fibrosis. Glycobiology 2005, 15:747-775.
101. Zhang H. Concerns of using sialidase fusion protein as an experimental drug to combat seasonal and pandemic influenza. J. Antimicrob. Chemother. 2008, 62:219-223.