The rescue and selection of thermally stable type O vaccine candidate strains of foot-and-mouth disease virus.


Journal

Archives of virology
ISSN: 1432-8798
Titre abrégé: Arch Virol
Pays: Austria
ID NLM: 7506870

Informations de publication

Date de publication:
Aug 2021
Historique:
received: 23 09 2020
accepted: 26 03 2021
pubmed: 19 5 2021
medline: 17 7 2021
entrez: 18 5 2021
Statut: ppublish

Résumé

Inactivated foot-and-mouth disease virus (FMDV) vaccines have been used widely to control foot-and-mouth disease (FMD). However, the virions (146S) of this virus are easily dissociated into pentamer subunits (12S), which limits the immune protective efficacy of inactivated vaccines when the temperature is higher than 30 °C. A cold-chain system can maintain the quality of the vaccines, but such systems are usually not reliable in limited-resource settings. Thus, it is imperative to improve the thermostability of vaccine strains to guarantee the quality of the vaccines. In this study, four recombinant FMDV strains containing single or multiple amino acid substitutions in the structural proteins were rescued using a previously constructed FMDV type O full-length infectious clone (pO/DY-VP1). We found that single or multiple amino acid substitutions in the structural proteins affected viral replication to different degrees. Furthermore, the heat and acid stability of the recombinant viruses was significantly increased when compared with the parental virus. Three thermally stable recombinant viruses (rHN/DY-VP1

Identifiants

pubmed: 34003358
doi: 10.1007/s00705-021-05100-3
pii: 10.1007/s00705-021-05100-3
doi:

Substances chimiques

Vaccines, Inactivated 0
Viral Structural Proteins 0
Viral Vaccines 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2131-2140

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.

Références

Alexandersen S, Zhang Z, Donaldson AI, Garland AJ (2003) The pathogenesis and diagnosis of foot-and-mouth disease. J Comp Pathol 129(1):1–36. https://doi.org/10.1016/s0021-9975(03)00041-0
doi: 10.1016/s0021-9975(03)00041-0 pubmed: 12859905
Brown F (2003) The history of research in foot-and-mouth disease. Virus Res 91(1):3–7. https://doi.org/10.1016/s0168-1702(02)00268-x
doi: 10.1016/s0168-1702(02)00268-x pubmed: 12527434
Sobrino F, Saiz M, Jimenez-Clavero MA, Nunez JI, Rosas MF, Baranowski E, Ley V (2001) Foot-and-mouth disease virus: a long known virus, but a current threat. Vet Res 32(1):1–30. https://doi.org/10.1051/vetres:2001106
doi: 10.1051/vetres:2001106 pubmed: 11254174
Doel TR, Baccarini PJ (1981) Thermal stability of foot-and-mouth disease virus. Adv Virol 70(1):21–32. https://doi.org/10.1007/BF01320790
doi: 10.1007/BF01320790
Doel TR, Chong WK (1982) Comparative immunogenicity of 146S, 75S and 12S particles of foot-and-mouth disease virus. Arch Virol 73(2):185–191. https://doi.org/10.1007/BF01314726
doi: 10.1007/BF01314726 pubmed: 6293410
Curry S, Abrams CC, Fry E, Crowther JC, Belsham GJ, Stuart DI, King AM (1995) Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J Virol 69(1):430–438. https://doi.org/10.1128/JVI.69.1.430-438.1995
doi: 10.1128/JVI.69.1.430-438.1995 pubmed: 7983739 pmcid: 188591
Newman JF, Rowlands DJ, Brown F (1973) A physico-chemical sub-grouping of the mammalian picornaviruses. J Gen Virol 18(2):171–180. https://doi.org/10.1099/0022-1317-18-2-171
doi: 10.1099/0022-1317-18-2-171 pubmed: 4351695
Vázquez-Calvo A, Caridi F, Sobrino F, Martín-Acebes MA (2014) An increase in acid resistance of foot-and-mouth disease virus capsid is mediated by a tyrosine replacement of the VP2 histidine previously associated with VP0 cleavage. J Virol 88(5):3039–3042. https://doi.org/10.1128/JVI.03222-13
doi: 10.1128/JVI.03222-13 pubmed: 24352460 pmcid: 3958075
Kitching P, Hammond J, Jeggo M, Charleston B, Paton D, Rodriguez L, Heckert R (2007) Global FMD control–is it an option? Vaccine 25(30):5660–5664. https://doi.org/10.1016/j.vaccine.2006.10.052
doi: 10.1016/j.vaccine.2006.10.052 pubmed: 17126959
Hunter P (1996) The performance of southern African territories serotypes of foot and mouth disease antigen in oil-adjuvanted vaccines. Rev Sci Tech 15 (3):913-922. https://doi.org/10.20506/rst.15.3.954
Parida S (2009) Vaccination against foot-and-mouth disease virus: strategies and effectiveness. Expert Rev Vaccines 8(3):347–365. https://doi.org/10.1586/14760584.8.3.347
doi: 10.1586/14760584.8.3.347 pubmed: 19249976
Cox SJ, Aggarwal N, Statham RJ, Barnett PV (2003) Longevity of antibody and cytokine responses following vaccination with high potency emergency FMD vaccines. Vaccine 21(13–14):1336–1347. https://doi.org/10.1016/s0264-410x(02)00691-6
doi: 10.1016/s0264-410x(02)00691-6 pubmed: 12615428
Doel TR (2003) FMD vaccines. Virus Res 91(1):81–99. https://doi.org/10.1016/s0168-1702(02)00261-7
doi: 10.1016/s0168-1702(02)00261-7 pubmed: 12527439
Hall MD, Knowles NJ, Wadsworth J, Rambaut A, Woolhouse ME (2013) Reconstructing geographical movements and host species transitions of foot-and-mouth disease virus serotype SAT 2. mBio 4 (5):e00591-00513. https://doi.org/10.1128/mBio.00591-13
Schlehuber LD, McFadyen IJ, Shu Y, Carignan J, Duprex WP, Forsyth WR, Ho JH, Kitsos CM, Lee GY, Levinson DA, Lucier SC, Moore CB, Nguyen NT, Ramos J, Weinstock BA, Zhang J, Monagle JA, Gardner CR, Alvarez JC (2011) Towards ambient temperature-stable vaccines: the identification of thermally stabilizing liquid formulations for measles virus using an innovative high-throughput infectivity assay. Vaccine 29(31):5031–5039. https://doi.org/10.1016/j.vaccine.2011.04.079
doi: 10.1016/j.vaccine.2011.04.079 pubmed: 21616113
Chen X, Fernando GJ, Crichton ML, Flaim C, Yukiko SR, Fairmaid EJ, Corbett HJ, Primiero CA, Ansaldo AB, Frazer IH, Brown LE, Kendall MA (2011) Improving the reach of vaccines to low-resource regions, with a needle-free vaccine delivery device and long-term thermostabilization. J Control Release 152(3):349–355. https://doi.org/10.1016/j.jconrel.2011.02.026
doi: 10.1016/j.jconrel.2011.02.026 pubmed: 21371510
Das P (2004) Revolutionary vaccine technology breaks the cold chain. Lancet Infect Dis 4(12):719. https://doi.org/10.1016/s1473-3099(04)01222-8
doi: 10.1016/s1473-3099(04)01222-8 pubmed: 15593445
Wang G, Cao RY, Chen R, Mo L, Han JF, Wang X, Xu X, Jiang T, Deng YQ, Lyu K, Zhu SY, Qin ED, Tang R, Qin CF (2013) Rational design of thermostable vaccines by engineered peptide-induced virus self-biomineralization under physiological conditions. Proc Natl Acad Sci USA 110(19):7619–7624. https://doi.org/10.1073/pnas.1300233110
doi: 10.1073/pnas.1300233110 pubmed: 23589862 pmcid: 3651461
Mateo R, Luna E, Rincon 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(24):12232–12240. https://doi.org/10.1128/JVI.01553-08
doi: 10.1128/JVI.01553-08 pubmed: 18829763 pmcid: 2593342
Kotecha A, Seago J, Scott K, Burman A, Loureiro S, Ren J, Porta C, Ginn HM, Jackson T, Perez-Martin E, Siebert CA, Paul G, Huiskonen JT, Jones IM, Esnouf RM, Fry EE, Maree FF, Charleston B, Stuart DI (2015) Structure-based energetics of protein interfaces guides foot-and-mouth disease virus vaccine design. Nat Struct Mol Biol 22(10):788–794. https://doi.org/10.1038/nsmb.3096
doi: 10.1038/nsmb.3096 pubmed: 26389739 pmcid: 5985953
Scott KA, Kotecha A, Seago J, Ren J, Fry EE, Stuart DI, Charleston B, Maree FF (2017) SAT2 Foot-and-Mouth Disease Virus Structurally Modified for Increased Thermostability. J Virol 91(10):e02312–e02316. https://doi.org/10.1128/JVI.02312-16
doi: 10.1128/JVI.02312-16 pubmed: 28298597 pmcid: 5411616
Cao WJ, Li PH, Bai XW, Lu ZJ, Sun P, Liu ZX (2010) Rescue and Identification of Virus Activity of Foot-and-Mouth Disease Virus Strain O/HN/93 from Full-length cDNA Clone. ACTA Agric Boreal Sin 25(3):32–37. https://doi.org/10.7668/hbnxb.2010.03.008
doi: 10.7668/hbnxb.2010.03.008
Sambrook J, Fritsch EF, Maniatis T (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, New York
Rieder E, Bunch T, Brown F, Mason PW (1993) Genetically engineered foot-and-mouth disease viruses with poly(C) tracts of two nucleotides are virulent in mice. J Virol 67(9):5139–5145. https://doi.org/10.1128/JVI.67.9.5139-5145.1993
doi: 10.1128/JVI.67.9.5139-5145.1993 pubmed: 8394441 pmcid: 237911
Pacheco JM, Henry TM, O’Donnell VK, Gregory JB, Mason PW (2003) Role of nonstructural proteins 3A and 3B in host range and pathogenicity of foot-and-mouth diseasevirus. J Virol 77(24):13017–13027. https://doi.org/10.1128/jvi.77.24.13017-13027.2003
doi: 10.1128/jvi.77.24.13017-13027.2003 pubmed: 14645558 pmcid: 296074
Knipe T, Rieder E, Baxt B, Ward G, Mason PW (1997) Characterization of synthetic foot-and-mouth disease virus provirions separates acid-mediated disassembly from infectivity. J Virol 71(4):2851–2856. https://doi.org/10.1128/JVI.71.4.2851-2856.1997
doi: 10.1128/JVI.71.4.2851-2856.1997 pubmed: 9060641 pmcid: 191410
Mateo R, Luna E, Mateu MG (2007) Thermostable variants are not generally represented in foot-and-mouth disease virus quasispecies. J Gen Virol 88(Pt 3):859–864. https://doi.org/10.1099/vir.0.82521-0
doi: 10.1099/vir.0.82521-0 pubmed: 17325358
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(4):1879–1887. https://doi.org/10.1128/JVI.01899-06
doi: 10.1128/JVI.01899-06 pubmed: 17151123
Mateo R, Diaz A, Baranowski E, Mateu MG (2003) Complete alanine scanning of intersubunit interfaces in a foot-and-mouth disease virus capsid reveals critical contributions of many side chains to particle stability and viral function. J Biol Chem 278(42):41019–41027. https://doi.org/10.1074/jbc.M304990200
doi: 10.1074/jbc.M304990200 pubmed: 12857761
Fowler VL, Bashiruddin JB, Maree FF, Mutowembwa P, Bankowski B, Gibson D, Cox S, Knowles N, Barnett PV (2011) Foot-and-mouth disease marker vaccine: cattle protection with a partial VP1 G-H loop deleted virus antigen. Vaccine 29(46):8405–8411. https://doi.org/10.1016/j.vaccine.2011.08.035
doi: 10.1016/j.vaccine.2011.08.035 pubmed: 21856354
OIE (2012) FMD. Manual of Standard for Diagnostic Test and Vaccine. OIE, Paris, pp 77–92
Shao J-J, Wong CK, Lin T, Lee SK, Cong G-Z, Sin FWY, Du J-Z, Gao S-D, Liu X-T, Cai X-P, Xie Y, Chang H-Y, Liu J-X (2011) Promising multiple-epitope recombinant vaccine against foot-and-mouth disease virus type O in swine. Clin Vaccine Immunol 18(1):143–149. https://doi.org/10.1128/CVI.00236-10
doi: 10.1128/CVI.00236-10 pubmed: 21084463
Barnett PV, Statham RJ, Vosloo W, Haydon DT (2003) Foot-and-mouth disease vaccine potency testing: determination and statistical validation of a model using a serological approach. Vaccine 21(23):3240–3248. https://doi.org/10.1016/s0264-410x(03)00219-6
doi: 10.1016/s0264-410x(03)00219-6 pubmed: 12804854
Bolwell C, Parry NR, Rowlands DJ (1992) Comparison between in vitro neutralization titres and in vivo protection against homologous and heterologous challenge induced by vaccines prepared from two serologically distinct variants of foot-and-mouth disease virus, serotype A22. J Gen Virol 73(3):727–731. https://doi.org/10.1099/0022-1317-73-3-727
doi: 10.1099/0022-1317-73-3-727 pubmed: 1312129
Brehm KE, Ferris NP, Lenk M, Riebe R, Haas B (2009) Highly sensitive fetal goat tongue cell line for detection and isolation of foot-and-mouth disease virus. J Clin Microbiol 47(10):3156–3160. https://doi.org/10.1128/JCM.00510-09
doi: 10.1128/JCM.00510-09 pubmed: 19656987 pmcid: 2756941
Luongo C, Winter CC, Collins PL, Buchholz UJ (2012) Increased genetic and phenotypic stability of a promising live-attenuated respiratory syncytial virus vaccine candidate by reverse genetics. J Virol 86(19):10792–10804. https://doi.org/10.1128/JVI.01227-12
doi: 10.1128/JVI.01227-12 pubmed: 22837193 pmcid: 3457269
Schulze P, Olechnowitz AF (1975) Electron microscopy studies on the proliferation of foot-and-mouth disease virus in cell cultures. III. Morphogenesis in cytoplasm. Arch Exp Veterinarmed 29(3):441–457
pubmed: 172043
Loladze VV, Ibarra-Molero B, Sanchez-Ruiz JM, Makhatadze GI (1999) Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface. Biochemistry 38(50):16419–16423. https://doi.org/10.1021/bi992271w
doi: 10.1021/bi992271w pubmed: 10600102
Rincón V, Rodríguez-Huete A, López-Argüello S, Ibarra-Molero B, Sanchez-Ruiz Jose M, Harmsen Michiel M, Mateu Mauricio G (2014) Identification of the structural basis of thermal lability of a virus provides a rationale for improved vaccines. Structure 22(11):1560–1570. https://doi.org/10.1016/j.str.2014.08.019
doi: 10.1016/j.str.2014.08.019 pubmed: 25308865
O’Donnell V, LaRocco M, Duque H, Baxt B (2005) Analysis of foot-and-mouth disease virus internalization events in cultured cells. J Virol 79(13):8506–8518. https://doi.org/10.1128/JVI.79.13.8506-8518.2005
doi: 10.1128/JVI.79.13.8506-8518.2005 pubmed: 15956593 pmcid: 1143741
Ganji VK, Biswal JK, Lalzampuia H, Basagoudanavar SH, Saravanan P, Tamil Selvan RP, Umapathi V, Reddy GR, Sanyal A, Dechamma HJ (2018) Mutation in the VP2 gene of P1–2A capsid protein increases the thermostability of virus-like particles of foot-and-mouth disease virus serotype O. Appl Microbiol Biotechnol 102(20):8883–8893. https://doi.org/10.1007/s00253-018-9278-9
doi: 10.1007/s00253-018-9278-9 pubmed: 30136205
Yuan H, Li P, Bao H, Sun P, Bai X, Bai Q, Li N, Ma X, Cao Y, Fu Y, Li K, Zhang J, Li D, Chen Y, Zhang J, Lu Z, Liu Z (2020) Engineering viable foot-and-mouth disease viruses with increased acid stability facilitate the development of improved vaccines. Appl Microbiol Biotechnol 104(4):1683–1694. https://doi.org/10.1007/s00253-019-10280-9
doi: 10.1007/s00253-019-10280-9 pubmed: 31900553 pmcid: 6985056

Auteurs

Ya Gao (Y)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Pinghua Li (P)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Xueqing Ma (X)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Xingwen Bai (X)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Pu Sun (P)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Ping Du (P)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Hong Yuan (H)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Yimei Cao (Y)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Kun Li (K)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Yuanfang Fu (Y)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Jing Zhang (J)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Huifang Bao (H)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Yingli Chen (Y)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Zhiyong Li (Z)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China.

Zengjun Lu (Z)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China. luzengjun@caas.cn.

Zaixin Liu (Z)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China. liuzaixin@caas.cn.

Dong Li (D)

State Key Laboratory of Veterinary Etiologic Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu, China. lidong@caas.cn.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH