Shift in oligosaccharide specificities of hemagglutinin and neuraminidase of influenza B viruses resistant to neuraminidase inhibitors

Glycoconjugate Journal

Volumn 27, Issue 3, 2010, Pages 321-327

  Mochalova, Larisa ^a,b   Bright, Rick ^c   Xu, Xiyan ^c   Korchagina, Elena ^a   Chinarev, Alexander ^a   Bovin, Nicolai ^a   Klimov, Alexander ^c  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

Drug resistance; Hemagglutinin; Influenza B virus; Neuraminidase; Neuraminidase inhibitor; Neuraminidase substrate specificity; Receptor binding specificity

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; INFLUENZA VIRUS SIALIDASE; N ACETYLNEURAMINIC ACID; OLIGOSACCHARIDE; OSELTAMIVIR; SIALIDASE INHIBITOR; UNCLASSIFIED DRUG; VIRUS SIALIDASE; ZANAMIVIR;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; ENZYME SPECIFICITY; INFLUENZA VIRUS B; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR BINDING;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; DOGS; DRUG RESISTANCE, VIRAL; HEMAGGLUTININS; INFLUENZA B VIRUS; NEURAMINIDASE; PROTEIN STRUCTURE, SECONDARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUBSTRATE SPECIFICITY;

AVES; INFLUENZA B VIRUS; ORTHOMYXOVIRIDAE;

EID: 77952097709     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-010-9280-7     Document Type: Article

References (38)

1. R Wagner M Matrosovich H-D Klenk 2002 Functional balance between hemagglutinin and neuraminidase in influenza virus infections Rev. Med. Virol. 12 159 166 10.1002/rmv.352 11987141 (Pubitemid 34516947)
2. M Matrosovich T Matrosovich T Gray NA Roberts H-D Klenk 2004 Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium J. Virol. 78 12665 12667 10.1128/JVI.78.22.12665-12667. 2004 1:CAS:528:DC%2BD2cXhtVWhu7fJ 15507653 (Pubitemid 39458784)
3. NV Kaverin AS Gambaryan NV Bovin IA Rudneva AA Shilov OM Khodova NL Varich BV Sinitsin NV Makarova EA Kropotkina 1998 Postreassortment changes in influenza A virus hemagglutinin restoring HA-NA functional match Virology 244 315 321 10.1006/viro.1998.9119 1:CAS:528:DyaK1cXjtFahsL0%3D 9601502 (Pubitemid 28384096)
4. SJ Baigent JW McCauley 2001 Glycosylation of haemagglutinin and stalk-lenth of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture Virus Res. 79 177 185 10.1016/S0168-1702(01)00272-6 1:CAS:528:DC%2BD3MXmsleitbg%3D 11551658 (Pubitemid 32817167)
5. LJ Mitnual MN Matrosovich MR Castrussi AB Tuzikov NV Bovin D Kobasa Y Kawaoka 2000 Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus J. Virol. 74 6015 6020 10.1128/JVI.74.13.6015-6020.2000 (Pubitemid 30412971)
6. IA Rudneva NA ll'yushina AA Shilov NL Varich BV Sinitsyn EA Kropotkina NV Kaverin 2003 Functional interaction of the influenza virus glycoproteins Mol. Biol. (Mosk.) 37 31 36 10.1023/A:1022372427314 1:CAS:528:DC%2BD3sXhtFSntro%3D (Pubitemid 36233440)
7. U Gimsa I Grötzinger J Gimsa 1996 Two evolutionary strategies of influenza viruses to escape host non-specific inhibitors: alteration of hemagglutinin or neuraminidase specificity Virus Res. 42 127 135 10.1016/0168-1702(96)01304-4 1:CAS:528:DyaK28XjsV2ntLg%3D 8806180 (Pubitemid 26198240)
8. Matrosovich, M.N., Klenk, H.-D., Kawaoka, Y.: Receptor specificity, host-range, and pathogenicity of influenza viruses. In: Kawaoka, Y. (ed.) Influenza virology: Current topics. Caister Academic, Norfolk (2006) (Pubitemid 44198580)
9. 2 and neuraminidase inhibitors: anti-influenza activity, mechanisms of resistance, and clinical effectiveness. In: Kawaoka, Y. (ed.) Influenza virology: Current topics. Caister Academic, Norfolk (2006)
10. NA Ilyushina IA Rudneva AA Shilov H-D Klenk NV Kaverin 2005 Postreassortment changes in a model system: HA-NA adjustment in an H3N2 avian-human reassortant influenza virus Arch. Virol. 150 1327 1338 10.1007/s00705-005-0490-4 10.1007/s00705-005-0490-4 1:CAS:528: DC%2BD2MXltl2mtr4%3D 15789269 (Pubitemid 40837321)
11. Y Shtyrya L Mochalova G Voznova I Rudneva A Shilov N Kaverin N Bovin 2009 Adjustment of receptor-binding and neuraminidase substrate specificities in avian-human reassortant influenza viruses Glycoconj. J. 26 99 109 10.1007/s10719-008-9169-x 1:CAS:528:DC%2BD1MXhtlOnsrY%3D 18661232
12. R Wagner T Wolf A Herwig S Pleschka H-D Klenk 2000 Interdependence of hemagglutinin glycosilation and neuraminidase as regulators of influenza growth: a study by reverse genetics J. Virol. 74 6316 6323 10.1128/JVI.74.14.6316-6323. 2000 1:CAS:528:DC%2BD3cXks1KmtL0%3D 10864641 (Pubitemid 30429796)
13. M Hughes M Matrosovich M Rodgers M McGregor Y Kawaoka 2000 Influenza A viruses lacking sialidase activity can undergo multiple cycles of replication in cell culture, eggs, or mice J. Virol. 74 5206 5212 10.1128/JVI.74.11.5206-5212. 2000 1:CAS:528:DC%2BD3cXjsVKnsr0%3D 10799596 (Pubitemid 30313861)
14. S Gulati DF Smith JM Air 2009 Deletions of neuraminidase and resistance to oseltamivir may be a consequence of restricted receptor specificity in recent H3N2 influenza viruses Virology J. 6 22 10.1186/1743-422X-6-22 10.1186/1743-422X-6-22
15. TG Sheu VM Deyde M Okomo-Adhiambo RJ Garten X Xu RA Bright EN Butler TR Wallis AI Klimov LV Gubareva 2008 Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to 2008 Antimicrob. Agents Chemother. 52 3284 3292 10.1128/AAC.00555-08 10.1128/AAC.00555-08 1:CAS:528:DC%2BD1cXhtF2gt77M 18625765
16. NL Dharan LV Gubareva JJ Meyer M Okomo-Adhiambo, et al. 2009 Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States JAMA 10.1001/jama.2009.294 19255110
17. LV Gubareva MN Matrosovich MK Brenner RC Bethell RG Webster 1998 Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus J. Infect. Dis. 178 1257 1262 10.1086/314440 1:STN:280: DyaK1cvltlCnsg%3D%3D 9780244 (Pubitemid 28523261)
18. L Mochalova A Gambaryan J Romanova A Tuzikov A Chinarev D Katinger H Katinger A Egorov N Bovin 2003 Receptor-binding properties of modern human influenza viruses primarily isolated in Vero and MDCK cells and chicken embryonated eggs Virology 313 473 480 10.1016/S0042-6822(03)00377-5 1:CAS:528:DC%2BD3sXmvVOqs70%3D 12954214 (Pubitemid 37040687)
19. L Mochalova V Kurova Y Styrya E Korchagina A Gambaryan I Belyanchikov N Bovin 2007 Oligosaccharide specificity of influenza H1N1 virus neuraminidases Arch. Virol. 152 2047 2057 10.1007/s00705-007-1024-z 1:CAS:528: DC%2BD2sXht1amtb3E 17680329 (Pubitemid 350112292)
20. LV Mochalova EY Korchagina VS Kurova JA Styria AS Gambaryan NV Bovin 2005 Fluorescent assay for studying the substrate specificity of neuraminidase Analyt. Biochem. 34 190 193 10.1016/j.ab.2005.02.019 (Pubitemid 40615736)
21. MN Janakiraman CL White WG Laver GM Air M Luo 1994 Structure of influenza virus neuraminidase B/Lee/40 complexed with sialic acid and dehydro analog at 1.8 Å resolution: implications for the catalytic mechanism Biochem. 33 8172 8179 10.1021/bi00193a002 1:CAS:528:DyaK2cXksFejt78%3D (Pubitemid 24241049)
22. MN Matrosovich LV Mochalova VP Marinina NE Byramova NV Bovin 1990 Synthetic polymeric sialoside inhibitors of influenza virus receptor-binding activity FEBS Lett. 272 209 212 10.1016/0014-5793(90)80486-3 1:CAS:528:DyaK3MXhslWnuw%3D%3D 1699804 (Pubitemid 20349019)
23. AS Gambarayn VP Marinina AB Tuzikov NV Bovin IA Rudneva BV Sinitsin AA Shilov MN Matrosovich 1998 Effect of host-dependent glycosylation of hemagglutinin on receptor-binding properties of H1N1 human influenza A virus grown in MDCK cells and in embryonated eggs Virology 247 170 177 10.1006/viro.1998.9224 (Pubitemid 28384008)
24. A Gambaryan JS Robertson MN Matrosovich 1999 Effect of egg-adaptation on the receptor-binding properties of human influenza A and B viruses Virology 258 232 239 10.1006/viro.1999.9732 1:CAS:528:DyaK1MXjslSksrs%3D 10366560 (Pubitemid 29390232)
25. G Xu G Horiike T Suzuki D Miyamoto H Kumihashi Y Suzuki 1996 A novel strain, B/Gifu/2/73, differs from other influenza B viruses in the receptor binding specificities toward sialo-sugar chain linkage Biochem. Biophys. Res. Communs 224 815 818 10.1006/bbrc.1996.1105 1:CAS:528:DyaK28Xks1Wjtbk%3D (Pubitemid 26278667)
26. Q Wang X Tian X Chen J Ma 2007 Structural basis for receptor specificity of influenza B virus hemagglutinin Proc. Nat. Acad. Sci. 104 16874 16879 10.1073/pnas.0708363104 1:CAS:528:DC%2BD2sXht1KgtLjI 17942670 (Pubitemid 350210958)
27. M Ohuchi R Ohuchi A Feldmann H-D Klenk 1997 Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety J. Virol. 71 8377 8384 1:CAS:528:DyaK2sXmvV2hs74%3D 9343193 (Pubitemid 27446417)
28. VP Mishin D Novikov FG Hayden LV Gubareva 2005 Effect of hemagglutinin glycosylation on influenza virus susceptibility to neuraminidase inhibitor J. Virol. 79 12416 12424 10.1128/JVI.79.19.12416-12424.2005 1:CAS:528: DC%2BD2MXhtVGlsL7M 16160169 (Pubitemid 41346104)
29. C Luo E Nobusawa K Nakajima 1999 An analysis of the role of neuraminidase in the receptor-binding activity of influenza B virus: the inhibitory effect of zanamivir on haemadsorption J. Gen. Virol. 80 2969 2976 1:CAS:528: DyaK1MXnt1yrsr4%3D 10580059 (Pubitemid 29504670)
30. LV Gubareva MS Nedyalkova DV Novikov KG Murti E Hoffmann FG Hayden 2002 A release-competent influenza A virus mutant lacking the coding capacity for the neuraminidase active site J. Gen. Virol. 83 2683 2692 1:CAS:528: DC%2BD38XosF2jsLs%3D 12388803 (Pubitemid 35276967)
31. AS Gambaryan AB Tuzikov VE Piskarev SS Yamnikova DK Lvov JS Robertson NV Bovin MN Matrosovich 1997 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) Virology 232 345 350 10.1006/viro.1997.8572 1:CAS:528:DyaK2sXjvFamurY%3D 9191848 (Pubitemid 27293578)
32. J Romanova D Katinger B Ferko R Voglauer L Mochalova N Bovin W Lim H Katinger A Egorov 2003 Distinct host range of influenza H3N2 virus isolates in Vero and MDCK cells is determined by cell specific glycosylation pattern Virology 307 90 97 10.1016/S0042-6822(02)00064-8 1:CAS:528:DC%2BD3sXitlWnt74%3D 12667817 (Pubitemid 36349439)
33. K Kumari S Gulati DF Smith U Gulati RD Cummings GM Air 2007 Receptor-binding specificity of recent human H3N2 influenza viruses Virology J. 4 42 10.1186/1743-422X-4-42 10.1186/1743-422X-4-42 (Pubitemid 46817314)
34. D Kobasa S Kodihalli M Luo MR Castrucci I Donatelli Y Suzuki T Suzuki Y Kawaoka 1999 Amino acid resides contributing to the substrate specificity of the influenza A virus neuraminidase J. Virol. 73 6743 6751 1:CAS:528: DyaK1MXksFKnuro%3D 10400772 (Pubitemid 29327857)
35. Shtyrya, Y., Mochalova, L., Gambarayn, A., Korchagina, E., Xu, X., Klimov, A., Bovin, N.: Neuraminidases of H9N2 influenza viruses isolated from different hosts display various substrate specificity. In: Options for the control of influenza VI, pp. 64-65. International Medical, Atlanta (2008). Toronto, Ontario, Canada, 17-23 June 2007
36. JF Barros Jr DS Alviano MH Silva MD Wigg CS Alviano R Schauer JNSS Couceiro 2003 Characterization of sialidase from an influenza A (H3N2) virus strain: kinetic parameters and substrate specificity Intervirology 46 199 206 10.1159/000072428 10.1159/000072428 (Pubitemid 37040626)
37. U Gulati W Wu S Gulati K Kumari JL Waner JM Air 2005 Mismatched hemagglutinin and neuraminidase specificities in recent human H3N2 influenza viruses Virology 339 12 20 10.1016/j.virol.2005.05.009 10.1016/j.virol.2005.05. 009 1:CAS:528:DC%2BD2MXntVOjtrY%3D 15950996 (Pubitemid 41096061)
38. M Matrosovich H-D Klenk 2003 Natural and synthetic sialic acid-containing inhibitors of influenza virus receptor-binding Rev. Med. Virol. 13 85 97 10.1002/rmv.372 10.1002/rmv.372 1:CAS:528:DC%2BD3sXislKgu7k%3D 12627392 (Pubitemid 36323672)