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01-02-2013 | Brief Report

Mass spectrometry analysis of influenza virus reassortant clones does not reveal an influence of other viral proteins on S-acylation of hemagglutinin

Authors: Marina V. Serebryakova, Larisa V. Kordyukova, Irina A. Rudneva, Ekaterina A. Kropotkina, Michael Veit, Lyudmila A. Baratova

Published in: Archives of Virology | Issue 2/2013

Abstract

Hemagglutinin (HA) of influenza virus is S-acylated with stearate at a transmembrane cysteine and with palmitate at two cytoplasmic cysteines. The amount of stearate varies from 35 (in avian strains) to 12% (in human strains), although the acylation region exhibits only minor or even no amino acid differences between HAs. To address whether matrix proteins and neuraminidase affect stearoylation of HA, we used mass spectrometry to analyze laboratory reassortants containing avian virus HA and the internal proteins from a human virus. Only minor fluctuations in the amount of stearate were observed, implying that other viral proteins do not affect acylation of HA.

Ali A, Avalos RT, Ponimaskin E, Nayak DP (2000) Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J Virol 74:8709–8719PubMedCrossRef

Calder LJ, Wasilewski S, Berriman JA, Rosenthal PB (2010) Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci USA 107:10685–10690PubMedCrossRef

Chen BJ, Takeda M, Lamb RA (2005) Influenza virus hemagglutinin (h3 subtype) requires palmitoylation of its cytoplasmic tail for assembly: m1 proteins of two subtypes differ in their ability to support assembly. J Virol 79:13673–13684PubMedCrossRef

Furuse Y, Suzuki A, Kamigaki T, Oshitani H (2009) Evolution of the M gene of the influenza A virus in different host species: large-scale sequence analysis. Virol J 6:67PubMedCrossRef

Ilyushina NA, Rudneva IA, Shilov AA, Klenk HD, Kaverin NV (2005) Postreassortment changes in a model system: HA-NA adjustment in an H3N2 avian-human reassortant influenza virus. Arch Virol 150:1327–1338PubMedCrossRef

Kaverin NV, Matrosovich MN, Gambaryan AS, Rudneva IA, Shilov AA, Varich NL, Makarova NV, Kropotkina EA, Sinitsin BV (2000) Intergenic HA-NA interactions in influenza A virus: postreassortment substitutions of charged amino acid in the hemagglutinin of different subtypes. Virus Res 66:123–129PubMedCrossRef

Kordyukova LV, Serebryakova MV (2012) Mass spectrometric approaches to study enveloped viruses: new possibilities for structural biology and prophylactic medicine. Biochemistry (Mosc) 77:830–842CrossRef

Kordyukova LV, Serebryakova MV, Baratova LA, Veit M (2008) S acylation of the hemagglutinin of influenza viruses: mass spectrometry reveals site-specific attachment of stearic acid to a transmembrane cysteine. J Virol 82:9288–9292PubMedCrossRef

Kordyukova LV, Serebryakova MV, Baratova LA, Veit M (2010) Site-specific attachment of palmitate or stearate to cytoplasmic versus transmembrane cysteines is a common feature of viral spike proteins. Virology 398:49–56PubMedCrossRef

10.

Kordyukova LV, Serebryakova MV, Polyakov VY, Smirnova YuA, Fedorova NV, Baratova LA (2008) Influenza A virus M1 protein structure probed by proteolysis with bromelain. Protein Pept Lett 15:922–930PubMedCrossRef

11.

Kordyukova LV, Serebryakova MV, Polyansky AA, Kropotkina EA, Alexeevski AV, Veit M, Efremov RG, Filippova IY, Baratova LA (2011) Linker and/or transmembrane regions of influenza A/Group-1, A/Group-2 and type B virus hemagglutinins are packed differently within trimers. Biochim Biophys Acta 1808:1843–1854PubMedCrossRef

12.

Krylov PS, Rudneva IA, Timofeeva TA, Shilov AA, Ignat’eva AV, Govorkova EA, Kaverin NV (2009) Amino acid substitutions in the hemagglutinin of H5 influenza virus changing the antigenic specificity and virus virulence. Vopr Virusol 54:14–19PubMed

13.

Kuznetsova MA, Pekov UA, Ksenofontov AL, Kordyukova LV, Drutsa VL (2010) Estimation of the evolutionary stability of the Influenza A virus: prediction of variable regions in the domain structure of the M1 protein. Mosc Univ Biol Sci Bull 65:221–223CrossRef

14.

Linder ME, Deschenes RJ (2007) Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 8:74–84PubMedCrossRef

15.

Naeve CW, Williams D (1990) Fatty acids on the A/Japan/305/57 influenza virus hemagglutinin have a role in membrane fusion. Embo J 9:3857–3866PubMed

16.

Reid AH, Fanning TG, Janczewski TA, McCall S, Taubenberger JK (2002) Characterization of the 1918 “Spanish” influenza virus matrix gene segment. J Virol 76:10717–10723PubMedCrossRef

17.

Reverey H, Veit M, Ponimaskin E, Schmidt MF (1996) Differential fatty acid selection during biosynthetic S-acylation of a transmembrane protein (HEF) and other proteins in insect cells (Sf9) and in mammalian cells (CV1). J Biol Chem 271:23607–23610PubMedCrossRef

18.

Rossman JS, Jing X, Leser GP, Balannik V, Pinto LH, Lamb RA (2010) Influenza virus m2 ion channel protein is necessary for filamentous virion formation. J Virol 84:5078–5088PubMedCrossRef

19.

Rossman JS, Lamb RA (2011) Influenza virus assembly and budding. Virology 411:229–236PubMedCrossRef

20.

Rudneva IA, Kovaleva VP, Varich NL, Farashyan VR, Gubareva LV, Yamnikova SS, Popova IA, Presnova VP, Kaverin NV (1993) Influenza A virus reassortants with surface glycoprotein genes of the avian parent viruses: effects of HA and NA gene combinations on virus aggregation. Arch Virol 133:437–450PubMedCrossRef

21.

Rudneva IA, Timofeeva TA, Shilov AA, Kochergin-Nikitsky KS, Varich NL, Ilyushina NA, Gambaryan AS, Krylov PS, Kaverin NV (2007) Effect of gene constellation and postreassortment amino acid change on the phenotypic features of H5 influenza virus reassortants. Arch Virol 152:1139–1145PubMedCrossRef

22.

Ruigrok RW, Barge A, Durrer P, Brunner J, Ma K, Whittaker GR (2000) Membrane interaction of influenza virus M1 protein. Virology 267:289–298PubMedCrossRef

23.

Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ (2006) The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443:45–49PubMedCrossRef

24.

Russell RJ, Kerry PS, Stevens DJ, Steinhauer DA, Martin SR, Gamblin SJ, Skehel JJ (2008) Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc Natl Acad Sci USA 105(46):17736–17741PubMedCrossRef

25.

Sakai T, Ohuchi R, Ohuchi M (2002) Fatty acids on the A/USSR/77 influenza virus hemagglutinin facilitate the transition from hemifusion to fusion pore formation. J Virol 76:4603–4611PubMedCrossRef

26.

Scholtissek C, Stech J, Krauss S, Webster RG (2002) Cooperation between the hemagglutinin of avian viruses and the matrix protein of human influenza A viruses. J Virol 76:1781–1786PubMedCrossRef

27.

Serebryakova MV, Kordyukova LV, Baratova LA, Markushin SG (2006) Mass spectrometric sequencing and acylation character analysis of C-terminal anchoring segment from Influenza A hemagglutinin. Eur J Mass Spectrom (Chichester, Eng) 12:51–62CrossRef

28.

Serebryakova MV, Kordyukova LV, Semashko TA, Ksenofontov AL, Rudneva IA, Kropotkina EA, Filippova IY, Veit M, Baratova LA (2011) Influenza virus hemagglutinin spike neck architectures and interaction with model enzymes evaluated by MALDI-TOF mass spectrometry and bioinformatics tools. Virus Res 160:294–304PubMedCrossRef

29.

Thaa B, Herrmann A, Veit M (2009) The polybasic region is not essential for membrane binding of the matrix protein M1 of influenza virus. Virology 383:150–155PubMedCrossRef

30.

Thaa B, Herrmann A, Veit M (2010) Intrinsic cytoskeleton-dependent clustering of influenza virus M2 protein with hemagglutinin assessed by FLIM-FRET. J Virol 84:12445–12449PubMedCrossRef

31.

Veit M (2012) Palmitoylation of virus proteins. Biol Cell 104:1–23CrossRef

32.

Veit M, Ponimaskin E, Schmidt MF (2008) Analysis of S-acylation of proteins. Methods Mol Biol 446:163–182PubMedCrossRef

33.

Veit M, Schmidt MF (1993) Timing of palmitoylation of influenza virus hemagglutinin. FEBS Lett 336:243–247PubMedCrossRef

34.

Wagner R, Matrosovich M, Klenk HD (2002) Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev Med Virol 12:159–166PubMedCrossRef

35.

Wagner R, Herwig A, Azzouz N, Klenk HD (2005) Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity. J Virol 79:6449–6458PubMedCrossRef

36.

Zurcher T, Luo G, Palese P (1994) Mutations at palmitylation sites of the influenza virus hemagglutinin affect virus formation. J Virol 68:5748–5754PubMed

Title: Mass spectrometry analysis of influenza virus reassortant clones does not reveal an influence of other viral proteins on S-acylation of hemagglutinin
Authors: Marina V. Serebryakova
Larisa V. Kordyukova
Irina A. Rudneva
Ekaterina A. Kropotkina
Michael Veit
Lyudmila A. Baratova
Publication date: 01-02-2013
Publisher: Springer Vienna
Published in: Archives of Virology / Issue 2/2013
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-012-1510-9

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