Gene silencing of β-galactosamide α-2,6-sialyltransferase 1 inhibits human influenza virus infection of airway epithelial cells

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Wu, Dong ^a,b   Huang, Wenbo ^a   Wang, Yutao ^a   Guan, Wenda ^a   Li, Runfeng ^a   Yang, Zifeng ^a   Zhong, Nanshan ^a  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

Influenza virus; Receptors; RNAi; Sialyltransferase

Indexed keywords

BETA INTERFERON; CELL SURFACE RECEPTOR; DOUBLE STRANDED RNA; SMALL INTERFERING RNA; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; BETA GALACTOSAMIDE ALPHA 2,6 SIALYLTRANSFERASE 1 GENE; BIOSYNTHESIS; CELL SURFACE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG EFFICACY; EPITHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; INFLUENZA A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H9N2; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY EPITHELIUM; VIRUS ATTACHMENT; VIRUS GENOME; VIRUS PARTICLE; VIRUS STRAIN; WESTERN BLOTTING;

ANTIGENS, CD; CELL LINE; EPITHELIAL CELLS; GENE SILENCING; HUMANS; ORTHOMYXOVIRIDAE; RNA, SMALL INTERFERING; SIALYLTRANSFERASES; VIRAL LOAD; VIRUS INTERNALIZATION;

EID: 84899088609     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-14-78     Document Type: Article

References (40)

1. Public health. Surveillance of animal influenza for pandemic preparedness. Peiris JS, Poon LL, Guan Y, Science 2012 335 6073 1173 1174 10.1126/science.1219936 22345402
2. Situation updates-Pandemic (H1N1). 2009 [ http://www.who.int/csr/disease/ swineflu/en/
3. Emergence and spread of oseltamivir-resistant A (H1N1) influenza viruses in Oceania, South East Asia and South Africa. Hurt AC, Ernest J, Deng YM, Iannello P, Besselaar TG, Birch C, Buchy P, Chittaganpitch M, Chiu SC, Dwyer D, Antiviral Res 2009 83 1 90 93 10.1016/j.antiviral.2009.03.003 19501261
4. Selection of a single amino acid substitution in the hemagglutinin molecule by chicken eggs can render influenza A virus (H3) candidate vaccine ineffective. Kodihalli S, Justewicz DM, Gubareva LV, Webster RG, J Virol 1995 69 8 4888 4897 7609057
5. Interplay between influenza A virus and the innate immune signaling. Ehrhardt C, Seyer R, Hrincius ER, Eierhoff T, Wolff T, Ludwig S, Microbes Infect 2010 12 1 81 87 10.1016/j.micinf.2009.09.007 19782761
6. Human host factors required for influenza virus replication. Konig R, Stertz S, Zhou Y, Inoue A, Hoffmann HH, Bhattacharyya S, Alamares JG, Tscherne DM, Ortigoza MB, Liang Y, Gao Q, Andrews SE, Bandyopadhyay S, Jesus PD, Tu BP, Pache L, Shih C, Orth A, Bonamy G, Miraglia L, Ideker T, Sastre AG, Young JA, Palese P, Shaw ML, Chanda SK, Nature 2010 463 7282 813 817 10.1038/nature08699 20027183
7. Cellular networks involved in the influenza virus life cycle. Watanabe T, Watanabe S, Kawaoka Y, Cell Host Microbe 2010 7 6 427 439 10.1016/j.chom.2010. 05.008 20542247
8. Prevention of influenza pneumonitis by sialic acid-conjugated dendritic polymers. Landers JJ, Cao Z, Lee I, Piehler LT, Myc PP, Myc A, Hamouda T, Galecki AT, Baker JR, J Infect Dis 2002 186 9 1222 1230 10.1086/344316 12402191
9. Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 Influenza A and Influenza B viruses share a common high binding affinity for 6'-Sialyl(N-acetyllactosamine). Gambaryan AS, Tuzikov A, Piskarev V, Yamnikova S, Lvov D, Robertson J, Bovin N, Matrosovich M, Virology 1997 232 2 345 350 10.1006/viro.1997.8572 9191848
10. DAS181, a novel sialidase fusion protein, protects mice from lethal avian influenza H5N1 virus infection. Belser JA, Lu X, Szretter KJ, Jin X, Aschenbrenner LM, Lee A, Hawley S, Malakhov MP, Yu M, Fang F, J Infect Dis 2007 196 10 1493 1499 10.1086/522609 18008229
11. The human sialyltransferase family. Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, Samyn-Petit B, Julien S, Delannoy P, Biochimie 2001 83 8 727 737 10.1016/S0300-9084(01)01301-3 11530204
12. Primary structure of beta-galactoside alpha 2,6-sialyltransferase. Conversion of membrane-bound enzyme to soluble forms by cleavage of the NH2-terminal signal anchor. Weinstein J, Lee EU, McEntee K, Lai PH, Paulson JC, J Biol Chem 1987 262 36 17735 17743 3121604
13. Cell surface [alpha] 2, 6-sialylation affects adhesion of breast carcinoma cells. Lin S, Kemmner W, Grigull S, Schlag PM, Exp Cell Res 2002 276 1 101 110 10.1006/excr.2002.5521 11978012
14. Inhibition of Gal [beta] 1, 4GlcNAc [alpha] 2, 6 sialyltransferase expression by antisense-oligodeoxynucleotides. Kemmner W, Hohaus K, Schlag PM, FEBS Lett 1997 409 3 347 350 10.1016/S0014-5793(97)00543-7 9224687
15. Prophylactic and therapeutic effects of small interfering RNA targeting SARS coronavirus. Zheng B, Guan Y, Tang Q, Du C, Xie FY, He ML, Chan KW, Wong KL, Lader E, Woodle MC, Antivir Ther 2004 9 3 365 374 15259899
16. Modest but reproducible inhibition of human immunodeficiency virus type 1 infection in macrophages following LEDGFp75 silencing. Zielske SP, Stevenson M, J Virol 2006 80 14 7275 7280 10.1128/JVI.02470-05 16809334
17. Inhibition of virus replication by RNA interference. Joost Haasnoot P, Cupac D, Berkhout B, J Biomedic Sci 2003 10 6 607 616 10.1007/BF02256311
18. Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque. Li B, Tang Q, Cheng D, Qin C, Xie FY, Wei Q, Xu J, Liu Y, Zheng B, Woodle MC, Nature Med 2005 11 9 944 951 16116432
19. RNA interference of influenza virus production by directly targeting mRNA for degradation and indirectly inhibiting all viral RNA transcription. Ge Q, McManus MT, Nguyen T, Shen CH, Sharp PA, Eisen HN, Chen J, Proc Natl Acad Sci 2003 100 5 2718 2723 10.1073/pnas.0437841100 12594334
20. Inhibition of influenza virus production in virus-infected mice by RNA interference. Ge Q, Filip L, Bai A, Nguyen T, Eisen HN, Chen J, Proc Natl Acad Sci U S A 2004 101 23 8676 10.1073/pnas.0402486101 15173599
21. Prophylactic and therapeutic efficacy of a chimeric monoclonal antibody specific for H5 haemagglutinin against lethal H5N1 influenza. Prabhu N, Prabakaran M, Hongliang Q, He F, Ho HT, Qiang J, Goutama M, Lim A, Hanson BJ, Kwang J, Antivir Ther 2009 14 7 911 921 10.3851/IMP1413 19918095
22. Sialic acid and receptor expression on the respiratory tract in normal subjects and H5N1 and non-avian influenza patients. Nicholls JM, Peiris JS, Guan Y, Hong Kong Med J 2009 15 3 Suppl 4 16 20 19509432
23. Use of siRNAs to prevent and treat influenza virus infection. Ge Q, Eisen HN, Chen J, Virus Res 2004 102 1 37 42 10.1016/j.virusres.2004.01.013 15068878
24. Short interfering RNAs can induce unexpected and divergent changes in the levels of untargeted proteins in mammalian cells. Scacheri PC, Rozenblatt-Rosen O, Caplen NJ, Wolfsberg TG, Umayam L, Lee JC, Hughes CM, Shanmugam KS, Bhattacharjee A, Meyerson M, Proc Natl Acad Sci U S A 2004 101 7 1892 10.1073/pnas.0308698100 14769924
25. Effective replication of human influenza viruses in mice lacking a major alpha2,6 sialyltransferase. Glaser L, Conenello G, Paulson J, Palese P, Virus Res 2007 126 1-2 9 18 17313986
26. The generation of influenza-specific humoral responses is impaired in ST6Gal I-deficient mice. Zeng J, Joo HM, Rajini B, Wrammert JP, Sangster MY, Onami TM, J Immunol 2009 182 8 4721 4727 10.4049/jimmunol.0802833 19342648
27. H5N1 chicken influenza viruses display a high binding affinity for Neu5Acalpha2-3Galbeta1-4(6-HSO3)GlcNAc-containing receptors. Gambaryan A, Tuzikov A, Pazynina G, Webster R, Matrosovich M, Bovin N, Virology 2004 326 2 310 316 10.1016/j.virol.2004.06.002 15302215
28. Mouse β-galactoside α2, 3-sialyltransferases: comparison of in vitro substrate specificities and tissue specific expression. Kono M, Ohyama Y, Lee YC, Hamamoto T, Kojima N, Tsuji S, Glycobiology 1997 7 4 469 479 10.1093/glycob/7.4.469 9184827
29. Molecular cloning and functional expression of a fifth-type α2, 3-sialyltransferase (mST3Gal V: GM3 synthase). Kono M, Takashima S, Liu H, Inoue M, Kojima N, Young-Choon L, Hamamoto T, Tsuji S, Biochem Biophys Res Commun 1998 253 1 170 175 10.1006/bbrc.1998.9768 9875239
30. Effects of egg-adaptation on the receptor-binding properties of human influenza A and B viruses. Gambaryan A, Robertson J, Matrosovich M, Virology 1999 258 2 232 239 10.1006/viro.1999.9732 10366560
31. Virulence-associated substitution D222G in the hemagglutinin of 2009 pandemic influenza A (H1N1) virus affects receptor binding. Chutinimitkul S, Herfst S, Steel J, Lowen AC, Ye J, van Riel D, Schrauwen EJA, Bestebroer TM, Koel B, Burke DF, J Virol 2010 84 22 11802 11813 10.1128/JVI.01136-10 20844044
32. Substrate specificity and preparative use of recombinant rat ST3Gal III. Schwardt O, Gao GP, Visekruna T, Rabbani S, Gassmann E, Ernst DB, J Carbohydr Chem 2004 23 1 1 26 10.1081/CAR-120030021
33. Description of α2,3-(O)-sialyltransferase, rat, recombinant, S. frugiperda. [ http://www.millipore.com/catalogue/item/566227-100miu#
34. A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. Glaser L, Stevens J, Zamarin D, Wilson IA, García-Sastre A, Tumpey TM, Basler CF, Taubenberger JK, Palese P, J Virol 2005 79 17 11533 11536 10.1128/JVI.79.17.11533-11536.2005 16103207
35. Inhibition of H5N1 highly pathogenic influenza virus by suppressing a specific sialyltransferase. Monteerarat Y, Suptawiwat O, Boonarkart C, Uiprasertkul M, Auewarakul P, Viprakasit V, Arch Virol 2010 155 6 889 893 10.1007/s00705-010-0658-4 20383541
36. BLOCK-iT™ RNAi designer. [ http://rnaidesigner.invitrogen.com/ rnaiexpress/
37. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T, Nature 2001 411 6836 494 498 10.1038/35078107 11373684
38. Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides. Nobusawa E, Ishihara H, Morishita T, Sato K, Nakajima K, Virology 2000 278 2 587 596 10.1006/viro.2000.0679 11118381
39. Resialylated erythrocytes for assessment of the specificity of sialyloligosaccharide binding proteins. Paulson JC, Rogers GN, Methods Enzymol 1987 138 162 168 3600320
40. Payment P, Trudel M, Methods and Techniques in Virology New York: Marcel Dekker 1993