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Erschienen in: Archives of Virology 4/2014

01.04.2014 | Original Article

Selection and characterization of an acid-resistant mutant of serotype O foot-and-mouth disease virus

verfasst von: Te Liang, Decheng Yang, Mengmeng Liu, Chao Sun, Fang Wang, Jingfei Wang, Haiwei Wang, Shanshan Song, Guohui Zhou, Li Yu

Erschienen in: Archives of Virology | Ausgabe 4/2014

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Abstract

Foot-and-mouth disease virus (FMDV) loses infectivity and immunogenicity due to its disassembly in culture environments below pH 6.8. To study the molecular basis of viral resistance to acid-induced disassembly and improve the acid stability of inactivated FMD vaccines during the manufacturing process, type O FMDV mutants with increased resistance to acid inactivation were selected, and the genes encoding their capsid proteins were sequenced. Three amino acid substitutions (VP1 N17D, VP2 D86A, and VP4 S73N) were found in all of the mutants. When these substitutions were introduced into seven infectious FMDV clones alone or combined, a single amino acid substitution in the VP1 protein, N17D, which also appears in type C FMDV acid-resistant mutants, was found to be responsible for the increased resistance to acid inactivation for type O FMDV. In addition, although viral fitness was reduced under standard culture conditions, viral growth kinetics and virulence were not significantly altered in the rescued mutant virus rN17D with the VP1 N17D substitution. Importantly, the N17D substitution could confer improved immunogenicity to the mutant virus rN17D under acidic conditions compared with its parental virus O/YS/CHA/05. These results demonstrate that the N17D substitution in VP1 is the molecular determinant of the acid-resistant phenotype in type O FMDV, indicating the potential for use of this substitution to improve the acid stability of inactivated FMD vaccines during the vaccine production process.
Literatur
1.
Zurück zum Zitat Acharya R, Fry E, Stuart D, Fox G, Rowlands D, Brown F (1989) The three-dimensional structure of foot-and-mouth disease virus at 2.9 Å resolution. Nature 337:709–716PubMedCrossRef Acharya R, Fry E, Stuart D, Fox G, Rowlands D, Brown F (1989) The three-dimensional structure of foot-and-mouth disease virus at 2.9 Å resolution. Nature 337:709–716PubMedCrossRef
2.
Zurück zum Zitat Almela MJ, González ME, Carrasco L (1991) Inhibitors of poliovirus uncoating efficiently block the early membrane permeabilization induced by virus particles. J Virol 65:2572–2577PubMedCentralPubMed Almela MJ, González ME, Carrasco L (1991) Inhibitors of poliovirus uncoating efficiently block the early membrane permeabilization induced by virus particles. J Virol 65:2572–2577PubMedCentralPubMed
4.
Zurück zum Zitat Baranowski E, Molina N, Núñez JI, Sobrino F, Sáiz M (2003) Recovery of infectious foot-and-mouth disease virus from suckling mice after direct inoculation with in vitro-transcribed RNA. J Virol 77:11290–11295PubMedCentralPubMedCrossRef Baranowski E, Molina N, Núñez JI, Sobrino F, Sáiz M (2003) Recovery of infectious foot-and-mouth disease virus from suckling mice after direct inoculation with in vitro-transcribed RNA. J Virol 77:11290–11295PubMedCentralPubMedCrossRef
5.
Zurück zum Zitat Baxt B (1987) Effect of lysosomotropic compounds on early events in foot-and-mouth disease virus replication. Virus Res 7:257–271PubMedCrossRef Baxt B (1987) Effect of lysosomotropic compounds on early events in foot-and-mouth disease virus replication. Virus Res 7:257–271PubMedCrossRef
6.
Zurück zum Zitat Brown F, Cartwright B (1961) Dissociation of foot-and-mouth disease virus into its nucleic acid and protein components. Nature 192:1163–1164PubMedCrossRef Brown F, Cartwright B (1961) Dissociation of foot-and-mouth disease virus into its nucleic acid and protein components. Nature 192:1163–1164PubMedCrossRef
7.
Zurück zum Zitat Capstick P, Garland A, Chapman W, Masters R (1967) Factors affecting the production of foot-and-mouth disease virus in deep suspension cultures of BHK 21 clone 13 cells. J Hyg 65:273–280PubMedCentralPubMedCrossRef Capstick P, Garland A, Chapman W, Masters R (1967) Factors affecting the production of foot-and-mouth disease virus in deep suspension cultures of BHK 21 clone 13 cells. J Hyg 65:273–280PubMedCentralPubMedCrossRef
8.
Zurück zum Zitat Carrillo EC, Giachetti C, Campos RH (1984) Effect of lysosomotropic agents on the foot-and-mouth disease virus replication. Virology 135:542–545PubMedCrossRef Carrillo EC, Giachetti C, Campos RH (1984) Effect of lysosomotropic agents on the foot-and-mouth disease virus replication. Virology 135:542–545PubMedCrossRef
9.
Zurück zum Zitat Carrillo EC, Giachetti C, Campos R (1985) Early steps in FMDV replication: further analysis on the effects of chloroquine. Virology 147:118–125PubMedCrossRef Carrillo EC, Giachetti C, Campos R (1985) Early steps in FMDV replication: further analysis on the effects of chloroquine. Virology 147:118–125PubMedCrossRef
10.
Zurück zum Zitat Curry S, Abrams CC, Fry E, Crowther JC, Belsham GJ, Stuart DI, King A (1995) Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J Virol 69:430–438PubMedCentralPubMed Curry S, Abrams CC, Fry E, Crowther JC, Belsham GJ, Stuart DI, King A (1995) Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J Virol 69:430–438PubMedCentralPubMed
11.
Zurück zum Zitat Diez J, Dávila M, Escarmis C, Mateu M, Dominguez J, Perez J, Giralt E, Melero J, Domingo E (1990) Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J Virol 64:5519–5528PubMedCentralPubMed Diez J, Dávila M, Escarmis C, Mateu M, Dominguez J, Perez J, Giralt E, Melero J, Domingo E (1990) Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J Virol 64:5519–5528PubMedCentralPubMed
12.
Zurück zum Zitat Doel T, Baccarini P (1981) Thermal stability of foot-and-mouth disease virus. Arch Virol 70:21–32PubMedCrossRef Doel T, Baccarini P (1981) Thermal stability of foot-and-mouth disease virus. Arch Virol 70:21–32PubMedCrossRef
13.
Zurück zum Zitat Doel T, Chong W (1982) Comparative immunogenicity of 146S, 75S and 12S particles of foot-and-mouth disease virus. Arch Virol 73:185–191PubMedCrossRef Doel T, Chong W (1982) Comparative immunogenicity of 146S, 75S and 12S particles of foot-and-mouth disease virus. Arch Virol 73:185–191PubMedCrossRef
15.
Zurück zum Zitat Doel T (2005) Natural and vaccine induced immunity to FMD, Foot-and-mouth disease virus. Curr Top Microbiol Immunol 288:103–131PubMed Doel T (2005) Natural and vaccine induced immunity to FMD, Foot-and-mouth disease virus. Curr Top Microbiol Immunol 288:103–131PubMed
16.
Zurück zum Zitat Domingo E, Mateu MG, Martinez M, Dopazo J, Moya A, Sobrino F (1990) Genetic variability and antigenic diversity of foot-and-mouth disease virus. Appl Virol Res 2:233–266 Domingo E, Mateu MG, Martinez M, Dopazo J, Moya A, Sobrino F (1990) Genetic variability and antigenic diversity of foot-and-mouth disease virus. Appl Virol Res 2:233–266
17.
Zurück zum Zitat Domingo E, Biebricher CK, Eigen M, Holland JJ (2001) Quasispecies and RNA virus evolution: principles and consequences. Landes Bioscience, Georgetown Domingo E, Biebricher CK, Eigen M, Holland JJ (2001) Quasispecies and RNA virus evolution: principles and consequences. Landes Bioscience, Georgetown
18.
Zurück zum Zitat Domingo E, Baranowski E, Escarmís C, Sobrino F (2002) Foot-and-mouth disease virus. Comp Immunol Microbiol Infect Dis 25:297–308PubMedCrossRef Domingo E, Baranowski E, Escarmís C, Sobrino F (2002) Foot-and-mouth disease virus. Comp Immunol Microbiol Infect Dis 25:297–308PubMedCrossRef
19.
Zurück zum Zitat Domingo E, Escarmís C, Baranowski E, Ruiz-Jarabo CM, Carrillo E, Núñez JI, Sobrino F (2003) Evolution of foot-and-mouth disease virus. Virus Res 91:47–63PubMedCrossRef Domingo E, Escarmís C, Baranowski E, Ruiz-Jarabo CM, Carrillo E, Núñez JI, Sobrino F (2003) Evolution of foot-and-mouth disease virus. Virus Res 91:47–63PubMedCrossRef
20.
Zurück zum Zitat Domingo E, Ruiz-Jarabo C, Arias A, García-Arriaza J, Escarmís C, Sobrino F (2004) Quasispecies dynamics and evolution of foot-and-mouth disease virus. In: Sobrino F, Domingo E (eds) Foot-and-mouth disease. Current perspectives. Horizon Bioscience, Norfolk, pp 261–304CrossRef Domingo E, Ruiz-Jarabo C, Arias A, García-Arriaza J, Escarmís C, Sobrino F (2004) Quasispecies dynamics and evolution of foot-and-mouth disease virus. In: Sobrino F, Domingo E (eds) Foot-and-mouth disease. Current perspectives. Horizon Bioscience, Norfolk, pp 261–304CrossRef
21.
Zurück zum Zitat Domingo E, Martı′n V, Perales C, Grande-Pe′rez A, Garcı′a-Arriaza J, Arias A (2006) Quasispecies: concept and implications for virology. In: Domingo E (ed) Springer, Berlin, pp 51–82 Domingo E, Martı′n V, Perales C, Grande-Pe′rez A, Garcı′a-Arriaza J, Arias A (2006) Quasispecies: concept and implications for virology. In: Domingo E (ed) Springer, Berlin, pp 51–82
22.
Zurück zum Zitat Ellard FM, Drew J, Blakemore WE, Stuart DI, King AM (1999) Evidence for the role of His-142 of protein 1C in the acid-induced disassembly of foot-and-mouth disease virus capsids. J Gen Virol 80:1911–1918PubMed Ellard FM, Drew J, Blakemore WE, Stuart DI, King AM (1999) Evidence for the role of His-142 of protein 1C in the acid-induced disassembly of foot-and-mouth disease virus capsids. J Gen Virol 80:1911–1918PubMed
24.
Zurück zum Zitat Gutiérrez-Rivas M, Pulido MR, Baranowski E, Sobrino F, Sáiz M (2008) Tolerance to mutations in the foot-and-mouth disease virus integrin-binding RGD region is different in cultured cells and in vivo and depends on the capsid sequence context. J Gen Virol 89:2531–2539PubMedCrossRef Gutiérrez-Rivas M, Pulido MR, Baranowski E, Sobrino F, Sáiz M (2008) Tolerance to mutations in the foot-and-mouth disease virus integrin-binding RGD region is different in cultured cells and in vivo and depends on the capsid sequence context. J Gen Virol 89:2531–2539PubMedCrossRef
25.
Zurück zum Zitat Kärber G (1931) Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Arch Exp Pathol Pharmacol 162:480–483CrossRef Kärber G (1931) Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Arch Exp Pathol Pharmacol 162:480–483CrossRef
26.
Zurück zum Zitat Maree FF, Blignaut B, de Beer TA, Rieder E (2013) Analysis of SAT type foot-and-mouth disease virus capsid proteins and the identification of putative amino acid residues affecting virus stability. PLoS One 8:e61612PubMedCentralPubMedCrossRef Maree FF, Blignaut B, de Beer TA, Rieder E (2013) Analysis of SAT type foot-and-mouth disease virus capsid proteins and the identification of putative amino acid residues affecting virus stability. PLoS One 8:e61612PubMedCentralPubMedCrossRef
27.
Zurück zum Zitat Martín-Acebes MA, Rincón V, Armas-Portela R, Mateu MG, Sobrino F (2010) A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid lability and confer resistance to acid-dependent uncoating inhibition. J Virol 84:2902–2912PubMedCentralPubMedCrossRef Martín-Acebes MA, Rincón V, Armas-Portela R, Mateu MG, Sobrino F (2010) A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid lability and confer resistance to acid-dependent uncoating inhibition. J Virol 84:2902–2912PubMedCentralPubMedCrossRef
28.
Zurück zum Zitat Martín-Acebes MA, Saiz JC (2011) A West Nile virus mutant with increased resistance to acid-induced inactivation. J Gen Virol 92:831–840PubMedCrossRef Martín-Acebes MA, Saiz JC (2011) A West Nile virus mutant with increased resistance to acid-induced inactivation. J Gen Virol 92:831–840PubMedCrossRef
29.
Zurück zum Zitat Martín-Acebes MA, Vázquez-Calvo Á, Rincón V, Mateu MG, Sobrino F (2011) A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid resistance. J Virol 85:2733–2740PubMedCentralPubMedCrossRef Martín-Acebes MA, Vázquez-Calvo Á, Rincón V, Mateu MG, Sobrino F (2011) A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid resistance. J Virol 85:2733–2740PubMedCentralPubMedCrossRef
30.
Zurück zum Zitat Mateo R, Mateu MG (2007) Deterministic, compensatory mutational events in the capsid of foot-and-mouth disease virus in response to the introduction of mutations found in viruses from persistent infections. J Virol 81:1879–1887PubMedCentralPubMedCrossRef Mateo R, Mateu MG (2007) Deterministic, compensatory mutational events in the capsid of foot-and-mouth disease virus in response to the introduction of mutations found in viruses from persistent infections. J Virol 81:1879–1887PubMedCentralPubMedCrossRef
31.
Zurück zum Zitat Mateo R, Luna E, Rincón V, Mateu MG (2008) Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J Virol 82:12232–12240PubMedCentralPubMedCrossRef Mateo R, Luna E, Rincón V, Mateu MG (2008) Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J Virol 82:12232–12240PubMedCentralPubMedCrossRef
32.
Zurück zum Zitat Mateu M, Verdaguer N, Sobrino F, Domingo E (2004) Functional and structural aspects of the interaction of foot-and-mouth disease virus with antibodies. Foot and mouth disease: current perspectives, pp 223–260 Mateu M, Verdaguer N, Sobrino F, Domingo E (2004) Functional and structural aspects of the interaction of foot-and-mouth disease virus with antibodies. Foot and mouth disease: current perspectives, pp 223–260
33.
Zurück zum Zitat Mateu MG (1995) Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res 38:1–24PubMedCrossRef Mateu MG (1995) Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res 38:1–24PubMedCrossRef
34.
Zurück zum Zitat Mosser AG, Sgro J-Y, Rueckert RR (1994) Distribution of drug resistance mutations in type 3 poliovirus identifies three regions involved in uncoating functions. J Virol 68:8193–8201PubMedCentralPubMed Mosser AG, Sgro J-Y, Rueckert RR (1994) Distribution of drug resistance mutations in type 3 poliovirus identifies three regions involved in uncoating functions. J Virol 68:8193–8201PubMedCentralPubMed
35.
Zurück zum Zitat Nandi S, Suryanarayana V, Banumathi N, Sen A (1997) Biochemical characterization of FMDV A10 and A22 subtypes by PAGE and IEF. Comp Immunol Microbiol Infect Dis 20:95–99PubMedCrossRef Nandi S, Suryanarayana V, Banumathi N, Sen A (1997) Biochemical characterization of FMDV A10 and A22 subtypes by PAGE and IEF. Comp Immunol Microbiol Infect Dis 20:95–99PubMedCrossRef
36.
Zurück zum Zitat Newman J, Rowlands D, Brown F (1973) A physico-chemical sub-grouping of the mammalian picornaviruses. J Gen Virol 18:171–180PubMedCrossRef Newman J, Rowlands D, Brown F (1973) A physico-chemical sub-grouping of the mammalian picornaviruses. J Gen Virol 18:171–180PubMedCrossRef
37.
Zurück zum Zitat Pereira H (1981) Foot-and-mouth disease. In: Gibbs EPJ (ed) Virus disease of food animals, vol 2. Academic Press, London, pp 333–363 Pereira H (1981) Foot-and-mouth disease. In: Gibbs EPJ (ed) Virus disease of food animals, vol 2. Academic Press, London, pp 333–363
38.
Zurück zum Zitat Prchla E, Kuechler E, Blaas D, Fuchs R (1994) Uncoating of human rhinovirus serotype 2 from late endosomes. J Virol 68:3713–3723PubMedCentralPubMed Prchla E, Kuechler E, Blaas D, Fuchs R (1994) Uncoating of human rhinovirus serotype 2 from late endosomes. J Virol 68:3713–3723PubMedCentralPubMed
39.
Zurück zum Zitat Rodriguez LL, Grubman MJ (2009) Foot and mouth disease virus vaccines. Vaccine 27(Suppl 4):D90–D94PubMedCrossRef Rodriguez LL, Grubman MJ (2009) Foot and mouth disease virus vaccines. Vaccine 27(Suppl 4):D90–D94PubMedCrossRef
40.
Zurück zum Zitat Sobrino F, Domingo E (2001) Foot-and-mouth disease in Europe: FMD is economically the most important disease of farm animals. Its re-emergence in Europe is likely to have consequences that go beyond severe alterations of livestock production and trade. EMBO Rep 2:459–461PubMedCentralPubMedCrossRef Sobrino F, Domingo E (2001) Foot-and-mouth disease in Europe: FMD is economically the most important disease of farm animals. Its re-emergence in Europe is likely to have consequences that go beyond severe alterations of livestock production and trade. EMBO Rep 2:459–461PubMedCentralPubMedCrossRef
41.
Zurück zum Zitat Twomey T, France L, Hassard S, Burrage T, Newman J, Brown F (1995) Characterization of an acid-resistant mutant of foot-and-mouth disease virus. Virology 206:69–75PubMedCrossRef Twomey T, France L, Hassard S, Burrage T, Newman J, Brown F (1995) Characterization of an acid-resistant mutant of foot-and-mouth disease virus. Virology 206:69–75PubMedCrossRef
42.
Zurück zum Zitat Vázquez-Calvo Á, Caridi F, Rodriguez-Pulido M, Borrego B, Sáiz M, Sobrino F, Martín-Acebes MA (2012) Modulation of foot-and-mouth disease virus pH threshold for uncoating correlates with differential sensitivity to inhibition of cellular Rab GTPases and decreases infectivity in vivo. J General Virol 93:2382–2386CrossRef Vázquez-Calvo Á, Caridi F, Rodriguez-Pulido M, Borrego B, Sáiz M, Sobrino F, Martín-Acebes MA (2012) Modulation of foot-and-mouth disease virus pH threshold for uncoating correlates with differential sensitivity to inhibition of cellular Rab GTPases and decreases infectivity in vivo. J General Virol 93:2382–2386CrossRef
43.
Zurück zum Zitat van Vlijmen HW, Curry S, Schaefer M, Karplus M (1998) Titration calculations of foot-and-mouth disease virus capsids and their stabilities as a function of pH. J Mol Biol 275:295–308PubMedCrossRef van Vlijmen HW, Curry S, Schaefer M, Karplus M (1998) Titration calculations of foot-and-mouth disease virus capsids and their stabilities as a function of pH. J Mol Biol 275:295–308PubMedCrossRef
44.
Zurück zum Zitat Vasquez C, Denoya CD, La Torre JÈL, Palma EL (1979) Structure of foot-and-mouth disease virus capsid. Virology 97:195–200PubMedCrossRef Vasquez C, Denoya CD, La Torre JÈL, Palma EL (1979) Structure of foot-and-mouth disease virus capsid. Virology 97:195–200PubMedCrossRef
45.
Zurück zum Zitat Yang D, Tu Y, Wang H, Zhou G, Yu L (2009) Construction of infectious cDNA clone for PanAsia strain of FMDV serotype O. Chin J Prev Vet Med 31:1–5 Yang D, Tu Y, Wang H, Zhou G, Yu L (2009) Construction of infectious cDNA clone for PanAsia strain of FMDV serotype O. Chin J Prev Vet Med 31:1–5
46.
Zurück zum Zitat Yang D, Zhang C, Zhao L, Zhou G, Wang H, Yu L (2010) Identification of a conserved linear epitope on the VP1 protein of serotype O foot-and-mouth disease virus by neutralising monoclonal antibody 8E8. Virus Res 155:291–299PubMedCrossRef Yang D, Zhang C, Zhao L, Zhou G, Wang H, Yu L (2010) Identification of a conserved linear epitope on the VP1 protein of serotype O foot-and-mouth disease virus by neutralising monoclonal antibody 8E8. Virus Res 155:291–299PubMedCrossRef
Metadaten
Titel
Selection and characterization of an acid-resistant mutant of serotype O foot-and-mouth disease virus
verfasst von
Te Liang
Decheng Yang
Mengmeng Liu
Chao Sun
Fang Wang
Jingfei Wang
Haiwei Wang
Shanshan Song
Guohui Zhou
Li Yu
Publikationsdatum
01.04.2014
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 4/2014
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-013-1872-7

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