A histidine residue of the influenza virus hemagglutinin controls the pH dependence of the conformational change mediating membrane fusion

Journal of Virology

Volumn 88, Issue 22, 2014, Pages 13189-13200

  Mair, Caroline M ^a   Meyer, Tim ^b   Schneider, Katjana ^a   Huang, Qiang ^c   Veit, Michael ^b   Herrmann, Andreas ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HISTIDINE; HISTIDINE 184; INFLUENZA VIRUS HEMAGGLUTININ; UNCLASSIFIED DRUG; MUTANT PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL SURFACE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; INFLUENZA VIRUS A H5N1; MEMBRANE FUSION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PH MEASUREMENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTON TRANSPORT; RESIDUE ANALYSIS; VIRUS IDENTIFICATION; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; INFLUENZA A VIRUS (H5N1); METABOLISM; PH; PHYSIOLOGY; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS; VIRUS ENTRY;

HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS, H5N1 SUBTYPE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN CONFORMATION; VIRUS INTERNALIZATION;

EID: 84908374179     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01704-14     Document Type: Article

References (58)

1. Kielian M, Rey FA. 2006. Virus membrane-fusion proteins: More than one way to make a hairpin. Nat. Rev. Microbiol. 4:67-76. http://dx.doi.org/10.1038/nrmicro1326.
2. White JM, Delos SE, Brecher M, Schornberg K. 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43:189-219. http://dx.doi.org/10.1080/10409230802058320.
3. Harrison SC. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15: 690-698. http://dx.doi.org/10.1038/nsmb.1456.
4. Wilson I, Skehel J. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-373. http://dx.doi.org/10.1038/289366a0.
5. Bullough P, Hughson F, Skehel J, Wiley D. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43. http://dx.doi.org/10.1038/371037a0.
6. Kemble GW, Bodian DL, Rosé J, Wilson IA, White JM. 1992. Intermonomer disulfide bonds impair the fusion activity of influenza virus hemagglutinin. J. Virol. 66:4940-4950.
7. Godley L, Pfeifer J, Steinhauer D, Ely B, Shaw G, Kaufmann R, Suchanek E, Pabo C, Skehel JJ, Wiley DC. 1992. Introduction of intersubunit disulfide bonds in the membrane-distal region of the influenza hemagglutinin abolishes membrane fusion activity. Cell 68:635-645. http://dx.doi.org/10.1016/0092-8674(92)90140-8.
8. Huang Q, Opitz R, Knapp E-W, Herrmann A. 2002. Protonation and stability of the globular domain of influenza virus hemagglutinin. Biophys. J. 82:1050-1058. http://dx.doi.org/10.1016/S0006-3495(02)75464-7.
9. Böttcher C, Ludwig K, Herrmann A, Heel Van M, Stark H. 1999. Structure of influenza haemagglutinin at neutral and at fusogenic pH by electron cryo-microscopy. FEBS Lett. 463:255-259. http://dx.doi.org/10.1016/S0014-5793(99)01475-1.
10. Kampmann T, Mueller DS, Mark AE, Young PR, Kobe B. 2006. The role of histidine residues in low-pH-mediated viral membrane fusion. Structure 14:1481-1487. http://dx.doi.org/10.1016/j.str.2006.07.011.
11. 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. http://dx.doi.org/10.1126/science.1093373.
12. 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. http://dx.doi.org/10.1126/science.1124513.
13. Thoennes S, Li Z-N, Lee B-J, Langley WA, Skehel JJ, Russell RJ, Steinhauer DA. 2008. Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion. Virology 370:403-414. http://dx.doi.org/10.1016/j.virol.2007.08.035.
14. Warwicker J. 1989. A theoretical study of the acidification of the rhinovirus capsid. FEBS Lett. 257:403-407. http://dx.doi.org/10.1016/0014-5793(89)81582-0.
15. Warwicker J. 1992. Model for the differential stabilities of rhinovirus and poliovirus to mild acidic pH, based on electrostatics calculations. J. Mol. Biol. 223:247-257. http://dx.doi.org/10.1016/0022-2836(92)90729-4.
16. Grimsley GR, Scholtz JM, Pace CN. 2009. A summary of the measured pK values of the ionizable groups in folded proteins. Protein Sci. 18:247-251. http://dx.doi.org/10.1002/pro.19.
17. Pace CN, Grimsley GR, Scholtz JM. 2009. Protein ionizable groups: pK values and their contribution to protein stability and solubility. J. Biol. Chem. 284:13285-13289. http://dx.doi.org/10.1074/jbc.R800080200.
18. Reed ML, Yen H-L, DuBois RM, Bridges OA, Salomon R, Webster RG, Russell CJ. 2009. Amino acid residues in the fusion peptide pocket regulate the pH of activation of the H5N1 influenza virus hemagglutinin protein. J. Virol. 83:3568-3580. http://dx.doi.org/10.1128/JVI.02238-08.
19. Kalani MR, Moradi A, Moradi M, Tajkhorshid E. 2013. Characterizing a histidine switch controlling pH-dependent conformational changes of the influenza virus hemagglutinin. Biophys. J. 105:993-1003. http://dx.doi.org/10.1016/j.bpj.2013.06.047.
20. Leikina E, Ramos C, Markovic I, Zimmerberg J, Chernomordik LV. 2002. Reversible stages of the low-pH-triggered conformational change in influenza virus hemagglutinin. EMBO J. 21:5701-5710. http://dx.doi.org/10.1093/emboj/cdf559.
21. Fontana J, Cardone G, Heymann JB, Winkler DC, Steven AC. 2012. Structural changes in Influenza virus at low pH characterized by cryoelectron tomography. J. Virol. 86:2919-2929. http://dx.doi.org/10.1128/JVI.06698-11.
22. DuBois R, Zaraket H, Reddivari M, Heath R, White S, Russell C. 2011. Acid stability of the hemagglutinin protein regulates H5N1 influenza virus pathogenicity. PLoS Pathog. 7:e1002398. http://dx.doi.org/10.1371/journal.ppat.1002398.
23. Zaraket H, Bridges OA, Russell CJ. 2013. The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus replication and pathogenesis in mice. J. Virol. 87:4826-4834. http://dx.doi.org/10.1128/JVI.03110-12.
24. Reed ML, Bridges OA, Seiler P, Kim J-K, Yen H-L, Salomon R, Govorkova EA, Webster RG, Russell CJ. 2010. The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus pathogenicity and transmissibility in ducks. J. Virol. 84:1527-1535. http://dx.doi.org/10.1128/JVI.02069-09.
25. Zaraket H, Bridges O a, Duan S, Baranovich T, Yoon S-W, Reed ML, Salomon R, Webby RJ, Webster RG, Russell CJ. 2013. Increased acid stability of the hemagglutinin protein enhances H5N1 influenza virus growth in the upper respiratory tract but is insufficient for transmission in ferrets. J. Virol. 87:9911-9922. http://dx.doi.org/10.1128/JVI.01175-13.
26. Russell CJ. 11 July 2014. Acid-induced membrane fusion by the hemagglutinin protein and its role in influenza virus biology. Curr. Top. Microbiol. Immunol. http://dx.doi.org/10.1007/82_2014_393.
27. Stech J, Stech O, Herwig A, Altmeppen H, Hundt J, Gohrbandt S, Kreibich A, Weber S, Klenk H-D, Mettenleiter TC. 2008. Rapid and reliable universal cloning of influenza A virus genes by target-primed plasmid amplification. Nucleic Acids Res. 36:e139. http://dx.doi.org/10.1093/nar/gkn646.
28. Czudai-Matwich V, Schnare M, Pinkenburg O. 2013. A simple and fast system for cloning influenza A virus gene segments into pHW2000-and pCAGGS-based vectors. Arch. Virol. 158:2049-2058. http://dx.doi.org/10.1007/s00705-013-1697-4.
29. Kozerski C, Ponimaskin E, Schroth-Diez B, Schmidt MF, Herrmann A. 2000. Modification of the cytoplasmic domain of influenza virus hemagglutinin affects enlargement of the fusion pore. J. Virol. 74:7529-7537. http://dx.doi.org/10.1128/JVI.74.16.7529-7537.2000.
30. Schroth-Diez B, Ponimaskin E, Reverey H, Schmidt MF, Herrmann A. 1998. Fusion activity of transmembrane and cytoplasmic domain chimeras of the influenza virus glycoprotein hemagglutinin. J. Virol. 72:133-141.
31. Kaverin NV, Rudneva IA, Govorkova EA, Timofeeva TA, Shilov AA, Kochergin-Nikitsky KS, Krylov PS, Webster RG. 2007. Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. J. Virol. 81:12911-12917. http://dx.doi.org/10.1128/JVI.01522-07.
32. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck D, Field M, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau F, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher W, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiórkiewicz-Kuczera J, Yin D, Karplus M. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102: 3586-3616. http://dx.doi.org/10.1021/jp973084f.
33. Im W, Lee MS, Brooks CL. 2003. Generalized born model with a simple smoothing function. J. Comput. Chem. 24:1691-1702. http://dx.doi.org/10.1002/jcc.10321.
34. Kieseritzky G, Knapp E-W. 2008. Optimizing pKa computation in proteins with pH adapted conformations. Proteins 71:1335-1348. http://dx.doi.org/10.1002/prot.21820.
35. Daniels R, Downie J, Hay A. 1985. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 40:431-439. http://dx.doi.org/10.1016/0092-8674(85)90157-6.
36. Herfst S, Schrauwen EJA, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RAM. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534-1541. http://dx.doi.org/10.1126/science.1213362.
37. Zhang W, Shi Y, Lu X, Shu Y, Qi J, Gao GF. 2013. An airborne transmissible avian influenza H5 hemagglutinin seen at the atomic level. Science 340:1463-1467. http://dx.doi.org/10.1126/science.1236787.
38. Lim AP, Wong SK, Chan AH, Chan CE, Ooi EE, Hanson BJ. 2008. Epitope characterization of the protective monoclonal antibody VN04-2 shows broadly neutralizing activity against highly pathogenic H5N1. Virol. J. 5:80. http://dx.doi.org/10.1186/1743-422X-5-80.
39. Rachakonda PS, Veit M, Korte T, Ludwig K, Böttcher C, Huang Q, Schmidt MFG, Herrmann A. 2007. The relevance of salt bridges for the stability of the influenza virus hemagglutinin. FASEB J. 21:995-1002. http://dx.doi.org/10.1096/fj.06-7052hyp.
40. Puri A, Booy FP, Doms RW, White JM, Blumenthal R. 1990. Conformational changes and fusion activity of influenza virus hemagglutinin of the H2 and H3 subtypes: effects of acid pretreatment. J. Virol. 64:3824-3832.
41. Gruenke JA, Armstrong RT, Newcomb WW, Brown JC, White JM. 2002. New insights into the spring-loaded conformational change of influenza virus hemagglutinin. J. Virol. 76:4456-4466. http://dx.doi.org/10.1128/JVI.76.9.4456-4466.2002.
42. Kalthoff D, Globig A, Beer M. 2010. (Highly pathogenic) avian influenza as a zoonotic agent. Vet. Microbiol. 140:237-245. http://dx.doi.org/10.1016/j.vetmic.2009.08.022.
43. Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, Lipatov AS, Chan KH, Sturm-Ramirez KM, Cheung CL, Leung YH, Yuen KY, Webster RG, Peiris JS. 2004. H5N1 influenza: a protean pandemic threat. Proc. Natl. Acad. Sci. U. S. A. 101:8156-8161. http://dx.doi.org/10.1073/pnas.0402443101.
44. Qin Z-L, Zheng Y, Kielian M. 2009. Role of conserved histidine residues in the low-pH dependence of the Semliki Forest virus fusion protein. J. Virol. 83:4670-4677. http://dx.doi.org/10.1128/JVI.02646-08.
45. Boo I, te Wierik K, Douam F, Lavillette D, Poumbourios P, Drummer HE. 2012. Distinct roles in folding, CD81 receptor binding and viral entry for conserved histidine residues of hepatitis C virus glycoprotein E1 and E2. Biochem. J. 443:85-94. http://dx.doi.org/10.1042/BJ20110868.
46. Nelson S, Poddar S, Lin T-Y, Pierson TC. 2009. Protonation of individual histidine residues is not required for the pH-dependent entry of West Nile virus: evaluation of the "histidine switch" hypothesis. J. Virol. 83: 12631-12635. http://dx.doi.org/10.1128/JVI.01072-09.
47. Fritz R, Stiasny K, Heinz FX. 2008. Identification of specific histidines as pH sensors in flavivirus membrane fusion. J. Cell Biol. 183:353-361. http://dx.doi.org/10.1083/jcb.200806081.
48. Chanel-Vos C, Kielian M. 2004. A conserved histidine in the ij loop of the Semliki Forest virus E1 protein plays an important role in membrane fusion. J. Virol. 78:13543-13552. http://dx.doi.org/10.1128/JVI.78.24.13543-13552.2004.
49. Zhang W, Shi Y, Lu X, Shu Y, Qi J, Gao GF. 2013. Supplemental information: an airborne transmissible avian influenza H5 hemagglutinin seen at the atomic level. Science 340:1463-1467. http://dx.doi.org/10.1126/science.1236787.
50. Sun X, Shi Y, Lu X, He J, Gao F, Yan J, Qi J, Gao GF. 2013. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep. 3:769-778. http://dx.doi.org/10.1016/j.celrep.2013.01.025.
51. Wu Y, Wu Y, Tefsen B, Shi Y, Gao GF. 2014. Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol. 22:183-191. http://dx.doi.org/10.1016/j.tim.2014.01.010.
52. Lu X, Qi J, Shi Y, Wang M, Smith DF, Heimburg-Molinaro J, Zhang Y, Paulson JC, Xiao H, Gao GF. 2013. Structure and receptor binding specificity of hemagglutinin H13 from avian influenza A virus H13N6. J. Virol. 87:9077-9085. http://dx.doi.org/10.1128/JVI.00235-13.
53. Zhu X, Yu W, McBride R, Li Y, Chen L-M, Donis RO, Tong S, Paulson JC, Wilson IA. 2013. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc. Natl. Acad. Sci. U. S. A. 110:1458-1463. http://dx.doi.org/10.1073/pnas.1218509110.
54. Nakowitsch S, Wolschek M, Morokutti A, Ruthsatz T, Krenn BM, Ferko B, Ferstl N, Triendl A, Muster T, Egorov A, Romanova J. 2011. Mutations affecting the stability of the haemagglutinin molecule impair the immunogenicity of live attenuated H3N2 intranasal influenza vaccine candidates lacking NS1. Vaccine 29:3517-3524. http://dx.doi.org/10.1016/j.vaccine.2011.02.100.
55. Krenn BM, Egorov A, Romanovskaya-Romanko E, Wolschek M, Nakowitsch S, Ruthsatz T, Kiefmann B, Morokutti A, Humer J, Geiler J, Cinatl J, Michaelis M, Wressnigg N, Sturlan S, Ferko B, Batishchev OV, Indenbom AV, Zhu R, Kastner M, Hinterdorfer P, Kiselev O, Muster T, Romanova J. 2011. Single HA2 mutation increases the infectivity and immunogenicity of a live attenuated H5N1 intranasal influenza vaccine candidate lacking NS1. PLoS One 6:e18577. http://dx.doi.org/10.1371/journal.pone.0018577.
56. Murakami S, Horimoto T, Ito M, Takano R, Katsura H, Shimojima M, Kawaoka Y. 2012. Enhanced growth of influenza vaccine seed viruses in Vero cells mediated by broadening the optimal pH range for virus membrane fusion. J. Virol. 86:1405-1410. http://dx.doi.org/10.1128/JVI.06009-11.
57. Mair CM, Ludwig K, Herrmann A, Sieben C. 2014. Receptor binding andpHstability: how influenzaAvirus hemagglutinin affects host-specific virus infection. Biochim. Biophys. Acta 1838:1153-1168. http://dx.doi.org/10.1016/j.bbamem.2013.10.004.
58. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, Li C, Kawakami E, Yamada S, Kiso M, Suzuki Y, Maher EA, Neumann G, Kawaoka Y. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420-428. http://dx.doi.org/10.1038/nature10831.