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Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

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2018 Impact Factor: 7.575

Protein Cell    2016, Vol. 7 Issue (1) : 28-45    https://doi.org/10.1007/s13238-015-0193-x
REVIEW
Hemagglutinin-esterase-fusion (HEF) protein of influenza C virus
Mingyang Wang,Michael Veit()
Institute of Virology, Veterinary Medicine, Free University Berlin, Berlin, Germany
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Abstract

Influenza C virus, a member of the Orthomyxoviridae family, causes flu-like disease but typically only with mild symptoms. Humans are the main reservoir of the virus, but it also infects pigs and dogs. Very recently, influenza C-like viruses were isolated from pigs and cattle that differ from classical influenza C virus and might constitute a new influenza virus genus. Influenza C virus is unique since it contains only one spike protein, the hemagglutinin-esterase-fusion glycoprotein HEF that possesses receptor binding, receptor destroying and membrane fusion activities, thus combining the functions of Hemagglutinin (HA) and Neuraminidase (NA) of influenza A and B viruses. Here we briefly review the epidemiology and pathology of the virus and the morphology of virus particles and their genome. The main focus is on the structure of the HEF protein as well as on its co- and posttranslational modification, such as N-glycosylation,disulfide bond formation, S-acylation and proteolytic cleavage into HEF1 and HEF2 subunits. Finally, we describe the functions of HEF: receptor binding, esterase activity and membrane fusion.

Keywords influenza C virus      HEF      structure      receptor binding      esterase      membrane fusion     
Corresponding Author(s): Michael Veit   
Issue Date: 26 January 2016
 Cite this article:   
Mingyang Wang,Michael Veit. Hemagglutinin-esterase-fusion (HEF) protein of influenza C virus[J]. Protein Cell, 2016, 7(1): 28-45.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-015-0193-x
https://academic.hep.com.cn/pac/EN/Y2016/V7/I1/28
1 Alamgir AS, Matsuzaki Y, Hongo S, Tsuchiya E, Sugawara K, Muraki Y, Nakamura K (2000) Phylogenetic analysis of influenza C virus nonstructural (NS) protein genes and identification of the NS2 protein. J Gen Virol 81:1933–1940
https://doi.org/10.1099/0022-1317-81-8-1933
2 Apostolov K, Flewett TH (1969) Further observations on the structure of influenza viruses A and C. J Gen Virol 4:365–370
https://doi.org/10.1099/0022-1317-4-3-365
3 Bottcher-Friebertshauser E, Klenk HD, Garten W (2013) Activation of influenza viruses by proteases from host cells and bacteria in the human airway epithelium. Pathog Dis 69:87–100
https://doi.org/10.1111/2049-632X.12053
4 Brett K, Kordyukova LV, Serebryakova MV, Mintaev RR, Alexeevski AV, Veit M (2014) Site-specific S-acylation of influenza virus hemagglutinin: the location of the acylation site relative to the membrane border is the decisive factor for attachment of stearate. J Biol Chem 289:34978–34989
https://doi.org/10.1074/jbc.M114.586180
5 Brown IH, Harris PA, Alexander DJ (1995) Serological studies of influenza viruses in pigs in Great Britain 1991-2. Epidemiol Infect 114:511–520
https://doi.org/10.1017/S0950268800052225
6 Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43
https://doi.org/10.1038/371037a0
7 Calvo C, Garcia-Garcia ML, Borrell B, Pozo F, Casas I (2013) Prospective study of influenza C in hospitalized children. Pediatr Infect Dis J 32:916–919
8 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 79:13673–13684
https://doi.org/10.1128/JVI.79.21.13673-13684.2005
9 Cheong HK, Cheong C, Lee YS, Seong BL, Choi BS (1999) Structure of influenza virus panhandle RNA studied by NMR spectroscopy and molecular modeling. Nucleic Acids Res 27:1392–1397
https://doi.org/10.1093/nar/27.5.1392
10 Collin EA, Sheng Z, Lang Y, Ma W, Hause BM, Li F (2014) Cocirculation of two distinct genetic and antigenic lineages of proposed influenza D virus in cattle. J Virol 89:1036–1042
11 Collin EA, Sheng Z, Lang Y, Ma W, Hause BM, Li F (2015)Cocirculation of two distinct genetic and antigenic lineages of proposed influenza d virus in cattle. J Virol 89:1036–1042
https://doi.org/10.1128/JVI.02718-14
12 Compans RW, Bishop DH, Meier-Ewert H (1977) Structural components of influenza C virions. J Virol 21:658–665
13 Crescenzo-Chaigne B, van der Werf S (2007) Rescue of influenza Cvirus from recombinant DNA. J Virol 81:11282–11289
https://doi.org/10.1128/JVI.00910-07
14 Crescenzo-Chaigne B, Barbezange C, van der Werf S (2008) Non coding extremities of the seven influenza virus type C vRNA segments: effect on transcription and replication by the type C and type A polymerase complexes. Virol J 5:132
https://doi.org/10.1186/1743-422X-5-132
15 Cross KJ, Langley WA, Russell RJ, Skehel JJ, Steinhauer DA(2009) Composition and functions of the influenza fusion peptide. Protein Pept Lett 16:766–778
https://doi.org/10.2174/092986609788681715
16 Desselberger U, Racaniello VR, Zazra JJ, Palese P (1980) The 3’and 5’-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene 8:315–328
https://doi.org/10.1016/0378-1119(80)90007-4
17 Doms RW, Lamb RA, Rose JK, Helenius A (1993) Folding and assembly of viral membrane proteins. Virology 193:545–562
https://doi.org/10.1006/viro.1993.1164
18 Engel S, Scolari S, Thaa B, Krebs N, Korte T, Herrmann A, Veit M(2010) FLIM-FRETand FRAP reveal association of influenza virus haemagglutinin with membrane rafts. Biochem J 425:567–573
https://doi.org/10.1042/BJ20091388
19 Engel S, de Vries M, Herrmann A, Veit M (2012) Mutation of a rafttargeting signal in the transmembrane region retards transport of influenza virus hemagglutinin through the Golgi. FEBS Lett 586:277–282
https://doi.org/10.1016/j.febslet.2012.01.002
20 Flewett TH, Apostolov K (1967) A reticular structure in the wall of influenza C virus. J Gen Virol 1:297–304
21 Fodor E, Pritlove DC, Brownlee GG (1994) The influenza virus panhandle is involved in the initiation of transcription. J Virol 68:4092–4096
22 Formanowski F, Wharton SA, Calder LJ, Hofbauer C, Meier-Ewert H (1990) Fusion characteristics of influenza C viruses. J Gen Virol 71(Pt 5):1181–1188
https://doi.org/10.1099/0022-1317-71-5-1181
23 Francis T Jr, Quilligan JJ Jr, Minuse E (1950) Identification of another epidemic respiratory disease. Science 112:495–497
https://doi.org/10.1126/science.112.2913.495
24 Gao Q, Brydon EW, Palese P(2008) A seven-segmented influenza A virus expressing the influenza C virus glycoprotein HEF. J Virol 82:6419–6426
https://doi.org/10.1128/JVI.00514-08
25 Garten W, Will C, Buckard K, Kuroda K, Ortmann D, Munk K,Scholtissek C, Schnittler H, Drenckhahn D, Klenk HD (1992) Structure and assembly of hemagglutinin mutants of fowl plague virus with impaired surface transport. J Virol 66:1495–1505
26 Gerl MJ, Sampaio JL, Urban S, Kalvodova L, Verbavatz JM,Binnington B, Lindemann D, Lingwood CA, Shevchenko A,Schroeder C et al (2012) Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J Cell Biol 196:213–221
https://doi.org/10.1083/jcb.201108175
27 Gouarin S, Vabret A, Dina J, Petitjean J, Brouard J, Cuvillon-Nimal D, Freymuth F (2008) Study of influenza C virus infection in France. J Med Virol 80:1441–1446
https://doi.org/10.1002/jmv.21218
28 Greaves J, Chamberlain LH (2011) DHHC palmitoyl transferases:substrate interactions and (patho)physiology. Trends Biochem Sci 36:245–253
https://doi.org/10.1016/j.tibs.2011.01.003
29 Guo YJ, Jin FG, Wang P, Wang M, Zhu JM (1983) Isolation of influenza C virus from pigs and experimental infection of pigs with influenza C virus. J Gen Virol 64(Pt 1):177–182
30 Hamilton BS, Whittaker GR, Daniel S (2012) Influenza virusmediated membrane fusion: determinants of hemagglutinin fusogenic activity and experimental approaches for assessing virus fusion. Viruses 4:1144–1168
https://doi.org/10.3390/v4071144
31 Han X, Bushweller JH, Cafiso DS, Tamm LK (2001) Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat Struct Biol 8:715–720
https://doi.org/10.1038/90434
32 Harrison SC (2008) Viral membrane fusion. Nat Struct Mol Biol 15:690–698
https://doi.org/10.1038/nsmb.1456
33 Hause BM, Ducatez M, Collin EA, Ran Z, Liu R, Sheng Z, Armien A,Kaplan B, Chakravarty S, Hoppe ADet al (2013) Isolation of a novel swine influenza virus from Oklahoma in 2011 which is distantly related to human influenza C viruses. PLoS Pathog 9:e1003176
34 Herrler G, Klenk HD (1987) The surface receptor is a major determinant of the cell tropism of influenza C virus. Virology 159:102–108
https://doi.org/10.1016/0042-6822(87)90352-7
35 Herrler G, Klenk HD (1991) Structure and function of the HEF glycoprotein of influenza C virus. Adv Virus Res 40:213–234
https://doi.org/10.1016/S0065-3527(08)60280-8
36 Herrler G, Compans RW, Meier-Ewert H (1979) A precursor glycoprotein in influenza C virus. Virology 99:49–56
https://doi.org/10.1016/0042-6822(79)90035-7
37 Herrler G, Nagele A, Meier-Ewert H, Bhown AS, Compans RW (1981) Isolation and structural analysis of influenza C virion glycoproteins. Virology 113:439–451
https://doi.org/10.1016/0042-6822(81)90173-2
38 Herrler G, Rott R, Klenk HD, Muller HP, Shukla AK, Schauer R (1985) The receptor-destroying enzyme of influenza C virus is neuraminate-O-acetylesterase. EMBO J 4:1503–1506
39 Herrler G, Reuter G, Rott R, Klenk HD, Schauer R (1987) N-acetyl-9-O-acetylneuraminic acid, the receptor determinant for influenza Cvirus, is a differentiation marker on chicken erythrocytes. Bio Chem Hoppe-Seyler 368:451–454
https://doi.org/10.1515/bchm3.1987.368.1.451
40 Herrler G, Durkop I, Becht H, Klenk HD (1988a) The glycoprotein of influenza C virus is the haemagglutinin, esterase and fusion factor. J Gen Virol 69(Pt 4):839–846
41 Herrler G, Multhaup G, Beyreuther K, Klenk HD (1988b) Serine 71 of the glycoprotein HEF is located at the active site of the acetylesterase of influenza C virus. Arch Virol 102:269–274
42 Hewat EA, Cusack S, Ruigrok RW, Verwey C (1984) Low resolution structure of the influenza C glycoprotein determined by electron microscopy. J Mol Biol 175:175–193
https://doi.org/10.1016/0022-2836(84)90473-X
43 Hongo S, Sugawara K, Homma M, Nakamura K (1986a) The functions of oligosaccharide chains associated with influenza C viral glycoproteins. I. The formation of influenza C virus particles in the absence of glycosylation. Arch Virol 89:171–187
44 Hongo S, Sugawara K, Homma M, Nakamura K (1986b) The functions of oligosaccharide chains associated with influenza C viral glycoproteins. II. The role of carbohydrates in the antigenic properties of influenza C viral glycoproteins. Arch Virol 89:189–201
45 Hongo S, Sugawara K, Muraki Y, Matsuzaki Y, Takashita E, Kitame F, Nakamura K (1999) Influenza C virus CM2 protein is produced from a 374-amino-acid protein (P42) by signal peptidase cleavage. J Virol 73:46–50
46 Horimoto T, Kawaoka Y (1994) Reverse genetics provides direct evidence for a correlation of hemagglutinin cleavability and virulence of an avian influenza A virus. J Virol 68:3120–3128
47 Horimoto T, Gen F, Murakami S, Iwatsuki-Horimoto K, Kato K,Akashi H, Hisasue M, Sakaguchi M, Kawaoka Y, Maeda K (2014) Serological evidence of infection of dogs with human influenza viruses in Japan. Vet Rec 174:96
https://doi.org/10.1136/vr.101929
48 Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P (1987) Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci USA 84:8140–8144
https://doi.org/10.1073/pnas.84.22.8140
49 Huang RT, Rott R, Klenk HD (1981) Influenza viruses cause hemolysis and fusion of cells. Virology 110:243–247
https://doi.org/10.1016/0042-6822(81)90030-1
50 Joosting AC, Head B, Bynoe ML, Tyrrell DA (1968) Production of common colds in human volunteers by influenza C virus. Br Med J 4:153–154
https://doi.org/10.1136/bmj.4.5624.153
51 Kauppila J, Ronkko E, Juvonen R, Saukkoriipi A, Saikku P, Bloigu A,Vainio O, Ziegler T (2014) Influenza C virus infection in military recruits–symptoms and clinical manifestation. J Med Virol 86:879–885
https://doi.org/10.1002/jmv.23756
52 Kemble GW, Danieli T, White JM (1994) Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76:383–391
https://doi.org/10.1016/0092-8674(94)90344-1
53 Kitame F, Sugawara K, Ohwada K, Homma M (1982) Proteolytic activation of hemolysis and fusion by influenza C virus. Arch Virol 73:357–361
https://doi.org/10.1007/BF01318090
54 Klenk HD, Rott R, Orlich M, Blodorn J (1975) Activation of influenza A viruses by trypsin treatment. Virology 68:426–439
https://doi.org/10.1016/0042-6822(75)90284-6
55 Kordyukova LV, Serebryakova MV, Baratova LA, Veit M (2008) Sacylation of the hemagglutinin of influenza viruses: mass spectrometry reveals site-specific attachment of stearic acid to a transmembrane cysteine. J Virol 82:9288–9292
https://doi.org/10.1128/JVI.00704-08
56 Kraut J (1977) Serine proteases: structure and mechanism of catalysis. Annu Rev Biochem 46:331–358
https://doi.org/10.1146/annurev.bi.46.070177.001555
57 Lazarowitz SG, Choppin PW (1975) Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology 68:440–454
https://doi.org/10.1016/0042-6822(75)90285-8
58 Lenard J, Miller DK (1981) pH-Dependent hemolysis by influenza, Semliki, Forest virus, and Sendai virus. Virology 110:479–482
https://doi.org/10.1016/0042-6822(81)90079-9
59 Levental I, Grzybek M, Simons K (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49:6305–6316
https://doi.org/10.1021/bi100882y
60 Lorieau JL, Louis JM, Schwieters CD, Bax A (2012) pH-triggered,activated-state conformations of the influenza hemagglutinin fusion peptide revealed by NMR. Proc Natl Acad Sci USA 109:19994–19999
https://doi.org/10.1073/pnas.1213801109
61 Maeda T, Ohnishi S (1980) Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett 122:283–287
https://doi.org/10.1016/0014-5793(80)80457-1
62 Mair CM, Meyer T, Schneider K, Huang Q, Veit M, Herrmann A (2014) A histidine residue of the influenza virus hemagglutinin controls the pH dependence of the conformational change mediating membrane fusion. J Virol 88:13189–13200
https://doi.org/10.1128/JVI.01704-14
63 Manuguerra JC, Hannoun C (1992) Natural infection of dogs by influenza C virus. Res Virol 143:199–204
https://doi.org/10.1016/S0923-2516(06)80104-4
64 Manuguerra JC, Hannoun C, Aymard M (1992) Influenza C virus infection in France. J Infect 24:91–99
https://doi.org/10.1016/0163-4453(92)91150-A
65 Manuguerra JC, Hannoun C, Simon F, Villar E, Cabezas JA (1993)Natural infection of dogs by influenza C virus: a serological survey in Spain. New Microbiol 16:367–371
66 Martin LT, Verhagen A, Varki A (2003) Recombinant influenza Chemagglutinin-esterase as a probe for sialic acid 9-O-acetylation. Methods Enzymol 363:489–498
https://doi.org/10.1016/S0076-6879(03)01074-7
67 Matsuzaki M, Sugawara K, Adachi K, Hongo S, Nishimura H, Kitame F,Nakamura K (1992) Location of neutralizing epitopes on the hemagglutinin-esterase protein of influenza C virus. Virology 189:79–87
https://doi.org/10.1016/0042-6822(92)90683-G
68 Matsuzaki Y, Mizuta K, Sugawara K, Tsuchiya E, Muraki Y, Hongo S,Suzuki H, Nishimura H (2003) Frequent reassortment among influenza C viruses. J Virol 77:871–881
https://doi.org/10.1128/JVI.77.2.871-881.2003
69 Matsuzaki Y, Katsushima N, Nagai Y, Shoji M, Itagaki T, Sakamoto M, Kitaoka S, Mizuta K, Nishimura H (2006) Clinical features of influenza C virus infection in children. J Infect Dis 193:1229–1235
https://doi.org/10.1086/502973
70 Matsuzaki Y, Abiko C, Mizuta K, Sugawara K, Takashita E, Muraki Y, Suzuki H, Mikawa M, Shimada S, Sato K et al (2007) Anationwide epidemic of influenza C virus infection in Japan in 2004. J Clin Microbiol 45:783–788
https://doi.org/10.1128/JCM.01555-06
71 Mayr J, Haselhorst T, Langereis MA, Dyason JC, Huber W, Frey B,Vlasak R, de Groot RJ, von Itzstein M(2008) Influenza C virus and bovine coronavirus esterase reveal a similar catalytic mechanism:new insights for drug discovery. Glycoconj J 25:393–399
https://doi.org/10.1007/s10719-007-9094-4
72 Melkonian KA, Ostermeyer AG, Chen JZ, Roth MG, Brown DA(1999) Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J Biol Chem 274:3910–3917
https://doi.org/10.1074/jbc.274.6.3910
73 Minuse E, Quilligan JJ Jr, Francis T Jr (1954) Type C influenza virus.I. Studies of the virus and its distribution. J Lab Clin Med 43:31–42
74 Muchmore EA, Varki A (1987) Selective inactivation of influenza Cesterase: a probe for detecting 9-O-acetylated sialic acids. Science 236:1293–1295
https://doi.org/10.1126/science.3589663
75 Muraki Y, Hongo S (2010) The molecular virology and reverse genetics of influenza C virus. Jpn J Infect Dis 63:157–165
76 Muraki Y, Hongo S, Sugawara K, Kitame F, Nakamura K (1996) Evolution of the haemagglutinin-esterase gene of influenza C virus. J Gen Virol 77(Pt 4):673–679
77 Muraki Y, Washioka H, Sugawara K, Matsuzaki Y, Takashita E,Hongo S (2004) Identification of an amino acid residue on influenza C virus M1 protein responsible for formation of the cordlike structures of the virus. J Gen Virol 85:1885–1893
https://doi.org/10.1099/vir.0.79937-0
78 Muraki Y, Murata T, Takashita E, Matsuzaki Y, Sugawara K, Hongo S(2007) A mutation on influenza C virus M1 protein affects virion morphology by altering the membrane affinity of the protein. J Virol 81:8766–8773
https://doi.org/10.1128/JVI.00075-07
79 Naeve CW, Williams D (1990) Fatty acids on the A/Japan/305/57 influenza virus hemagglutinin have a role in membrane fusion. EMBO J 9:3857–3866
80 Nagele A, Meier-Ewert H (1984) Influenza-C-virion-associated RNA-dependent RNA-polymerase activity. Biosci Rep 4:703–706
https://doi.org/10.1007/BF01121024
81 Naim HY, Amarneh B, Ktistakis NT, Roth MG (1992) Effects of altering palmitylation sites on biosynthesis and function of the influenza virus hemagglutinin. J Virol 66:7585–7588
82 Nakada S, Creager RS, Krystal M, Aaronson RP, Palese P (1984a)Influenza C virus hemagglutinin: comparison with influenza A and B virus hemagglutinins. J Virol 50:118–124
83 Nakada S, Creager RS, Krystal M, Palese P (1984b) Complete nucleotide sequence of the influenza C/California/78 virus nucleoprotein gene. Virus Res 1:433–441
84 Nakada S, Graves PN, Desselberger U, Creager RS, Krystal M,Palese P (1985) Influenza C virus RNA 7 codes for a nonstructural protein. J Virol 56:221–226
85 Nakada S, Graves PN, Palese P (1986) The influenza C virus NS gene: evidence for a spliced mRNA and a second NS gene product (NS2 protein). Virus Res 4:263–273
https://doi.org/10.1016/0168-1702(86)90005-5
86 Nerome K, Nakayama M, Ishida M (1979) Established cell line sensitive to influenza C virus. J Gen Virol 43:257–259
https://doi.org/10.1099/0022-1317-43-1-257
87 Neumann G, Kawaoka Y(2006)Host range restriction and pathogenicity in the context of influenza pandemic. Emerg Infect Dis 12:881–886
https://doi.org/10.3201/eid1206.051336
88 Nishimura H, Hara M, Sugawara K, Kitame F, Takiguchi K, Umetsu Y, Tonosaki A, Nakamura K (1990) Characterization of the cordlike structures emerging from the surface of influenza C virusinfected cells. Virology 179:179–188
https://doi.org/10.1016/0042-6822(90)90287-2
89 Nishimura H, Hongo S, Sugawara K, Muraki Y, Kitame F, Washioka H, Tonosaki A, Nakamura K (1994) The ability of influenza C virus to generate cord-like structures is influenced by the gene coding for M protein. Virology 200:140–147
https://doi.org/10.1006/viro.1994.1172
90 O’Callaghan RJ, Loughlin M, Labat DD, Howe C (1977) Properties of influenza C virus grown in cell culture. J Virol 24:875–882
91 Oeffner F, Klenk HD, Herrler G (1999) The cytoplasmic tail of the influenza C virus glycoprotein HEF negatively affects transport to the cell surface. J Gen Virol 80(Pt 2):363–369
92 Ohuchi M, Ohuchi R, Mifune K (1982) Demonstration of hemolytic and fusion activities of influenza C virus. J Virol 42:1076–1079
93 Ohwada K, Kitame F, Sugawara K, Nishimura H, Homma M,Nakamura K (1987) Distribution of the antibody to influenza C virus in dogs and pigs in Yamagata Prefecture, Japan. Microbiol Immunol 31:1173–1180
https://doi.org/10.1111/j.1348-0421.1987.tb01351.x
94 Pachler K, Mayr J, Vlasak R (2010) A seven plasmid-based system for the rescue of influenza C virus. J Mol Genet Med 4:239–246
95 Pekosz A, Lamb RA (1998) Influenza C virus CM2 integral membrane glycoprotein is produced from a polypeptide precursor by cleavage of an internal signal sequence. Proc Natl Acad Sci USA 95:13233–13238
https://doi.org/10.1073/pnas.95.22.13233
96 Pekosz A, Lamb RA (1999) Cell surface expression of biologically active influenza C virus HEF glycoprotein expressed from cDNA. J Virol 73:8808–8812
97 Peng G, Hongo S, Muraki Y, Sugawara K, Nishimura H, Kitame F,Nakamura K (1994) Genetic reassortment of influenza C viruses in man. J Gen Virol 75(Pt 12):3619–3622
98 Pfeifer JB, Compans RW (1984) Structure of the influenza C glycoprotein gene as determined from cloned DNA. Virus Res 1:281–296
https://doi.org/10.1016/0168-1702(84)90017-0
99 Pleschka S, Klenk HD, Herrler G (1995) The catalytic triad of the influenza C virus glycoprotein HEF esterase: characterization by site-directed mutagenesis and functional analysis. J Gen Virol 76(Pt 10):2529–2537
100 Robertson JS (1979) 5’ and 3’ terminal nucleotide sequences of the RNA genome segments of influenza virus. Nucleic Acids Res 6:3745–3757
https://doi.org/10.1093/nar/6.12.3745
101 Rogers GN, Herrler G, Paulson JC, Klenk HD (1986) Influenza C virus uses 9-O-acetyl-N-acetylneuraminic acid as a high affinity receptor determinant for attachment to cells. J Biol Chem 261:5947–5951
102 Rosenthal PB, Zhang X, Formanowski F, Fitz W, Wong CH, Meier-Ewert H, Skehel JJ, Wiley DC (1998) Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 396:92–96
https://doi.org/10.1038/23974
103 Rossman JS, Lamb RA (2011) Influenza virus assembly and budding. Virology 411:229–236
https://doi.org/10.1016/j.virol.2010.12.003
104 Rossman JS, Jing X, Leser GP, Lamb RA (2010) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902–913
https://doi.org/10.1016/j.cell.2010.08.029
105 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 76:4603–4611
https://doi.org/10.1128/JVI.76.9.4603-4611.2002
106 Salez N, Melade J, Pascalis H, Aherfi S, Dellagi K, Charrel RN,Carrat F, de Lamballerie X(2014) Influenza C virus high seroprevalence rates observed in 3 different population groups. J Infect 69:182–189
https://doi.org/10.1016/j.jinf.2014.03.016
107 Schwegmann-Wessels C, Herrler G (2006) Sialic acids as receptor determinants for coronaviruses. Glycoconj J 23:51–58
https://doi.org/10.1007/s10719-006-5437-9
108 Segal MS, Bye JM, Sambrook JF, Gething MJ (1992) Disulfide bond formation during the folding of influenza virus hemagglutinin. J Cell Biol 118:227–244
https://doi.org/10.1083/jcb.118.2.227
109 Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569
https://doi.org/10.1146/annurev.biochem.69.1.531
110 Speranskaia AS, Mel’nikova NV, Belenkin MS, Dmitriev AA, Oparina N, Kudriavtseva AV (2012) Genetic diversity and evolution of the influenza C virus. Genetika 48:797–805
111 Steinhauer DA, Wharton SA, Wiley DC, Skehel JJ (1991) Deacylation of the hemagglutinin of influenza A/Aichi/2/68 has no effect on membrane fusion properties. Virology 184:445–448
https://doi.org/10.1016/0042-6822(91)90867-B
112 Stewart SM, Pekosz A (2012) The influenza C virus CM2 protein can alter intracellular pH, and its transmembrane domain can substitute for that of the influenza A virus M2 protein and support infectious virus production. J Virol 86:1277–1281
https://doi.org/10.1128/JVI.05681-11
113 Stieneke-Grober A, Vey M, Angliker H, Shaw E, Thomas G, Roberts C, Klenk HD, Garten W (1992) Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J 11:2407–2414
114 Sugawara K, Ohuchi M, Nakamura K, Homma M (1981) Effects of various proteases on the glycoprotein composition and the infectivity of influenza C virus. Arch Virol 68:147–151
https://doi.org/10.1007/BF01314445
115 Szepanski S, Gross HJ, Brossmer R, Klenk HD, Herrler G (1992) A single point mutation of the influenza C virus glycoprotein (HEF) changes the viral receptor-binding activity. Virology 188:85–92
https://doi.org/10.1016/0042-6822(92)90737-A
116 Szepanski S, Veit M, Pleschka S, Klenk HD, Schmidt MF, Herrler G(1994) Post-translational folding of the influenza C virus glycoprotein HEF: defective processing in cells expressing the cloned gene. J Gen Virol 75(Pt 5):1023–1030
https://doi.org/10.1099/0022-1317-75-5-1023
117 Takashita E, Muraki Y, Sugawara K, Asao H, Nishimura H, Suzuki K,Tsuji T, Hongo S, Ohara Y, Kawaoka Y et al (2012) Intrinsic temperature sensitivity of influenza C virus hemagglutininesterase-fusion protein. J Virol 86:13108–13111
https://doi.org/10.1128/JVI.01925-12
118 Taylor RM (1949) Studies on survival of influenza virus between epidemics and antigenic variants of the virus. Am J Public Health N Health 39:171–178
https://doi.org/10.2105/AJPH.39.2.171
119 Taylor RM (1951) A further note on 1233 influenza C virus. Archiv fur die gesamte Virusforschung 4:485–500
https://doi.org/10.1007/BF01241168
120 Thomas JK, Noppenberger J (2007) Avian influenza: a review. Am JHealth Syst Pharm (AJHP) 64:149–165
https://doi.org/10.2146/ajhp060181
121 Trebbien R, Larsen LE, Viuff BM (2011) Distribution of sialic acid receptors and influenza A virus of avian and swine origin in experimentally infected pigs. Virol J 8:434
https://doi.org/10.1186/1743-422X-8-434
122 Ujike M, Nakajima K, Nobusawa E (2004) Influence of acylation sites of influenza B virus hemagglutinin on fusion pore formation and dilation. J Virol 78:11536–11543
https://doi.org/10.1128/JVI.78.21.11536-11543.2004
123 Veit M (2012) Palmitoylation of virus proteins. Biol Cell 104:493–515
https://doi.org/10.1111/boc.201200006
124 Veit M, Schmidt MF (1993) Timing of palmitoylation of influenza virus hemagglutinin. FEBS Lett 336:243–247
https://doi.org/10.1016/0014-5793(93)80812-9
125 Veit M, Thaa B (2011) Association of influenza virus proteins with membrane rafts. Adv Virol 2011:370606
126 Veit M, Herrler G, Schmidt MF, Rott R, Klenk HD (1990) The hemagglutinating glycoproteins of influenza B and C viruses are acylated with different fatty acids. Virology 177:807–811
https://doi.org/10.1016/0042-6822(90)90554-5
127 Veit M, Kretzschmar E, Kuroda K, Garten W, Schmidt MF, Klenk HD,Rott R (1991) Site-specific mutagenesis identifies three cysteine residues in the cytoplasmic tail as acylation sites of influenza virus hemagglutinin. J Virol 65:2491–2500
128 Veit M, Reverey H, Schmidt MF (1996) Cytoplasmic tail length influences fatty acid selection for acylation of viral glycoproteins. Biochem J 318(Pt 1):163–172
129 Veit M, Serebryakova MV, Kordyukova LV (2013) Palmitoylation of influenza virus proteins. Biochem Soc Trans 41:50–55
https://doi.org/10.1042/BST20120210
130 Vlasak R, Krystal M, Nacht M, Palese P (1987) The influenza C virus glycoprotein (HE) exhibits receptor-binding (hemagglutinin) and receptor-destroying (esterase) activities. Virology 160:419–425
https://doi.org/10.1016/0042-6822(87)90013-4
131 Vlasak R, Luytjes W, Spaan W, Palese P (1988) Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. ProcNatl Acad Sci USA 85:4526–4529
https://doi.org/10.1073/pnas.85.12.4526
132 Wagaman PC, Spence HA, O’Callaghan RJ (1989) Detection of influenza C virus by using an in situ esterase assay. J Clin Microbiol 27:832–836
133 Wagner R, Herwig A, Azzouz N, Klenk HD (2005) Acylationmediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity. J Virol 79:6449–6458
https://doi.org/10.1128/JVI.79.10.6449-6458.2005
134 Waterson AP, Hurrell JM, Jensen KE (1963) The fine structure of influenza A, B and C viruses. Archiv fur die gesamte Virusforschung 12:487–495
https://doi.org/10.1007/BF01242156
135 Yamaoka M, Hotta H, Itoh M, Homma M (1991) Prevalence of antibody to influenza C virus among pigs in Hyogo Prefecture,Japan. J Gen Virol 72(Pt 3):711–714
136 Yamashita M, Krystal M, Palese P (1988) Evidence that the matrix protein of influenza C virus is coded for by a spliced mRNA. J Virol 62:3348–3355
137 Yamashita M, Krystal M, Palese P (1989) Comparison of the three large polymerase proteins of influenza A, B, and C viruses. Virology 171:458–466
https://doi.org/10.1016/0042-6822(89)90615-6
138 Youzbashi E, Marschall M, Chaloupka I, Meier-Ewert H (1996)Distribution of influenza C virus infection in dogs and pigs in Bavaria. Tierarztl Prax 24:337–342
139 Zeng Q, Langereis MA, van Vliet AL, Huizinga EG, de Groot RJ(2008) Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc Natl Acad Sci USA 105:9065–9069
https://doi.org/10.1073/pnas.0800502105
140 Zhang X, Rosenthal PB, Formanowski F, Fitz W, Wong CH, Meier-Ewert H, Skehel JJ, Wiley DC (1999) X-ray crystallographic determination of the structure of the influenza C virus haemagglutinin-esterase-fusion glycoprotein. Acta Crystallogr D Biol Crystallogr 55:945–961
https://doi.org/10.1107/S0907444999000232
141 Zhang J, Pekosz A, Lamb RA (2000) Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J Virol 74:4634–4644
https://doi.org/10.1128/JVI.74.10.4634-4644.2000
142 Zimmer G, Suguri T, Reuter G, Yu RK, Schauer R, Herrler G (1994) Modification of sialic acids by 9-O-acetylation is detected in human leucocytes using the lectin property of influenza C virus. Glycobiology 4:343–349
https://doi.org/10.1093/glycob/4.3.343
143 Zurcher T, Luo G, Palese P (1994) Mutations at palmitylation sites of the influenza virus hemagglutinin affect virus formation. J Virol 68:5748–5754
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