Efficacy of a trivalent hand, foot, and mouth disease vaccine against enterovirus 71 and coxsackieviruses A16 and A6 in mice

Viruses

Volumn 7, Issue 11, 2015, Pages 5919-5932

  Caine, Elizabeth A ^a   Fuchs, Jeremy ^b   Das, Subash C ^b   Partidos, Charalambos D ^b   Osorio, Jorge E ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Takeda Vaccines Inc   (United States)

Author keywords

AG129 mice; Coxsackievirus A16; Coxsackievirus A6; Enterovirus 71; Interferon; Mouse model; Trivalent vaccine

Indexed keywords

HFMD VACCINE; UNCLASSIFIED DRUG; VIRUS VACCINE; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COXSACKIEVIRUS A16; COXSACKIEVIRUS A6; ENTEROVIRUS 71; ENTEROVIRUS A; HAND FOOT AND MOUTH DISEASE; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS CHARACTERIZATION; VIRUS INACTIVATION; VIRUS LOAD; VIRUS NEUTRALIZATION; ADAPTATION; ANIMAL; CROSS PROTECTION; DISEASE MODEL; ENTEROVIRUS; GROWTH, DEVELOPMENT AND AGING; HAND, FOOT AND MOUTH DISEASE; IMMUNOLOGY; SURVIVAL ANALYSIS; VIRUS CULTURE;

ADAPTATION, BIOLOGICAL; ANIMALS; ANTIBODIES, VIRAL; CROSS PROTECTION; DISEASE MODELS, ANIMAL; ENTEROVIRUS; ENTEROVIRUS A, HUMAN; HAND, FOOT AND MOUTH DISEASE; MICE; SERIAL PASSAGE; SURVIVAL ANALYSIS; VIRAL VACCINES;

EID: 84947460208     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7112916     Document Type: Article

References (51)

1. Chong, P.; Liu, C.C.; Chow, Y.H.; Chou, A.H.; Klein, M. Review of enterovirus 71 vaccines. Clin. Infect. Dis. 2015, 60, 797-803. [CrossRef] [PubMed]
2. Osterback, R.; Vuorinen, T.; Linna, M.; Susi, P.; Hyypia, T.;Waris, M. Coxsackievirus a6 and hand, foot, and mouth disease, finland. Emerg. Infect. Dis. 2009, 15, 1485-1488. [CrossRef] [PubMed]
3. Zeng, M.; el Khatib, N.F.; Tu, S.; Ren, P.; Xu, S.; Zhu, Q.; Mo, X.; Pu, D.; Wang, X.; Altmeyer, R. Seroepidemiology of enterovirus 71 infection prior to the 2011 season in children in Shanghai. J. Clin. Virol. 2012, 53, 285-289. [CrossRef] [PubMed]
4. Nguyen, N.T.; Pham, H.V.; Hoang, C.Q.; Nguyen, T.M.; Nguyen, L.T.; Phan, H.C.; Phan, L.T.; Vu, L.N.; Tran Minh, N.N. Epidemiological and clinical characteristics of children who died from hand, foot and mouth disease in Vietnam, 2011. BMC Infect. Dis. 2014, 14, 341. [CrossRef] [PubMed]
5. Wu, Y.; Yeo, A.; Phoon, M.C.; Tan, E.L.; Poh, C.L.; Quak, S.H.; Chow, V.T. The largest outbreak of hand; foot and mouth disease in Singapore in 2008: The role of enterovirus 71 and coxsackievirus A strains. Int. J. Infect. Dis. 2010, 14, e1076-e1081. [CrossRef] [PubMed]
6. Akiyoshi, K.; Suga, T.; Mori, A. Enteroviruses in patients experiencing multiple episodes of hand, foot, and mouth disease in the same season in Kobe, Japan, 2011. Jpn. J. Infect. Dis. 2012, 65, 459-461. [CrossRef] [PubMed]
7. Kim, S.J.; Kim, J.H.; Kang, J.H.; Kim, D.S.; Kim, K.H.; Kim, K.H.; Kim, Y.H.; Chung, J.Y.; Bin, J.H.; Jung da, E.; et al. Risk factors for neurologic complications of hand, foot and mouth disease in the Republic of Korea, 2009. J. Korean Med. Sci. 2013, 28, 120-127. [CrossRef] [PubMed]
8. Fonseca, M.C.; Sarmiento, L.; Resik, S.; Martinez, Y.; Hung, L.H.; Morier, L.; Pinon, A.; Valdez, O.; Kouri, V.; Gonzalez, G. Coxsackievirus a6 and enterovirus 71 causing hand, foot and mouth disease in Cuba, 2011-2013. Arch Virol. 2014, 159, 2451-2455. [CrossRef] [PubMed]
9. Cabrerizo, M.; Tarrago, D.; Munoz-Almagro, C.; del Amo, E.; Dominguez-Gil, M.; Eiros, J.M.; Lopez-Miragaya, I.; Perez, C.; Reina, J.; Otero, A.; et al. Molecular epidemiology of enterovirus 71, coxsackievirus A16 and A6 associated with hand, foot and mouth disease in Spain. Clin. Microbiol. Infect. 2014, 20, O150-O156. [CrossRef] [PubMed]
10. Solomon, T.; Lewthwaite, P.; Perera, D.; Cardosa, M.J.; McMinn, P.; Ooi, M.H. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect. Dis. 2010, 10, 778-790. [CrossRef]
11. Lin, C.W.; Liu, C.C.; Lu, T.C.; Liu, S.J.; Chow, Y.H.; Chong, P.; Huang, M.H. Immunogenicity studies of bivalent inactivated virions of EV71/CVA16 formulated with submicron emulsion systems. BioMed Res. Int. 2014, 2014, 670506. [CrossRef] [PubMed]
12. Huang, W.C.; Huang, L.M.; Kao, C.L.; Lu, C.Y.; Shao, P.L.; Cheng, A.L.; Fan, T.Y.; Chi, H.; Chang, L.Y. Seroprevalence of enterovirus 71 and no evidence of crossprotection of enterovirus 71 antibody against the other enteroviruses in kindergarten children in Taipei city. J. Microbiol. Immunol. Infect. 2012, 45, 96-101. [CrossRef] [PubMed]
13. Li, R.; Liu, L.; Mo, Z.; Wang, X.; Xia, J.; Liang, Z.; Zhang, Y.; Li, Y.; Mao, Q.; Wang, J.; et al. An inactivated enterovirus 71 vaccine in healthy children. N. Engl. J. Med. 2014, 370, 829-837. [CrossRef] [PubMed]
14. Zhu, F.C.; Meng, F.Y.; Li, J.X.; Li, X.L.; Mao, Q.Y.; Tao, H.; Zhang, Y.T.; Yao, X.; Chu, K.; Chen, Q.H.; et al. Efficacy, safety, and immunology of an inactivated alum-adjuvant enterovirus 71 vaccine in children in china: A multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 2013, 381, 2024-2032. [CrossRef]
15. Mao, Q.; Cheng, T.; Zhu, F.; Li, J.; Wang, Y.; Li, Y.; Gao, F.; Yang, L.; Yao, X.; Shao, J.; et al. The cross-neutralizing activity of enterovirus 71 subgenotype c4 vaccines in healthy chinese infants and children. PLoS ONE 2013, 8, e79599. [CrossRef] [PubMed]
16. Liu, C.C.; Chow, Y.H.; Chong, P.; Klein, M. Prospect and challenges for the development of multivalent vaccines against hand, foot and mouth diseases. Vaccine 2014, 32, 6177-6182. [CrossRef] [PubMed]
17. Li, J.; Chang, J.; Liu, X.; Yang, J.; Guo, H.; Wei, W.; Zhang, W.; Yu, X.F. Protection from lethal challenge in a neonatal mouse model by circulating recombinant form coxsackievirus A16 vaccine candidates. J. Gen. Virol. 2014, 95, 1083-1093. [CrossRef] [PubMed]
18. Cai, Y.; Ku, Z.; Liu, Q.; Leng, Q.; Huang, Z. A combination vaccine comprising of inactivated enterovirus 71 and coxsackievirus a16 elicits balanced protective immunity against both viruses. Vaccine 2014, 32, 2406-2412. [CrossRef] [PubMed]
19. Wang,W.; Duo, J.; Liu, J.; Ma, C.; Zhang, L.;Wei, Q.; Qin, C. A mouse muscle-adapted enterovirus 71 strain with increased virulence in mice. Microbes Infect. 2011, 13, 862-870. [CrossRef] [PubMed]
20. Chen, Y.C.; Yu, C.K.; Wang, Y.F.; Liu, C.C.; Su, I.J.; Lei, H.Y. A murine oral enterovirus 71 infection model with central nervous system involvement. J. Gen. Virol. 2004, 85, 69-77. [CrossRef] [PubMed]
21. Khong, W.X.; Yan, B.; Yeo, H.; Tan, E.L.; Lee, J.J.; Ng, J.K.; Chow, V.T.; Alonso, S. A non-mouse-adapted enterovirus 71 (EV71) strain exhibits neurotropism, causing neurological manifestations in a novel mouse model of EV71 infection. J. Virol. 2012, 86, 2121-2131. [CrossRef] [PubMed]
22. Wang, Y.F.; Chou, C.T.; Lei, H.Y.; Liu, C.C.; Wang, S.M.; Yan, J.J.; Su, I.J.; Wang, J.R.; Yeh, T.M.; Chen, S.H.; et al. A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J. Virol. 2004, 78, 7916-7924. [CrossRef] [PubMed]
23. Yao, P.P.; Qian, L.; Xia, Y.; Xu, F.; Yang, Z.N.; Xie, R.H.; Li, X.; Liang, W.F.; Huang, X.X.; Zhu, Z.Y.; et al. Enterovirus 71-induced neurological disorders in young gerbils, meriones unguiculatus: Development and application of a neurological disease model. PLoS ONE 2012, 7, e51996. [CrossRef] [PubMed]
24. Fujii, K.; Nagata, N.; Sato, Y.; Ong, K.C.; Wong, K.T.; Yamayoshi, S.; Shimanuki, M.; Shitara, H.; Taya, C.; Koike, S. Transgenic mouse model for the study of enterovirus 71 neuropathogenesis. Proc. Natl. Acad. Sci. USA 2013, 110, 14753-14758. [CrossRef] [PubMed]
25. Yang, L.; Li, S.; Liu, Y.; Hou, W.; Lin, Q.; Zhao, H.; Xu, L.; He, D.; Ye, X.; Zhu, H.; et al. Construction and characterization of an infectious clone of coxsackievirus A6 that showed high virulence in neonatal mice. Virus Res. 2015, 210, 165-168. [CrossRef] [PubMed]
26. Mao, Q.; Wang, Y.; Gao, R.; Shao, J.; Yao, X.; Lang, S.; Wang, C.; Mao, P.; Liang, Z.; Wang, J. A neonatal mouse model of coxsackievirus A16 for vaccine evaluation. J. Virol. 2012, 86, 11967-11976. [CrossRef] [PubMed]
27. Yauch, L.E.; Zellweger, R.M.; Kotturi, M.F.; Qutubuddin, A.; Sidney, J.; Peters, B.; Prestwood, T.R.; Sette, A.; Shresta, S. A protective role for dengue virus-specific CD8+ T cells. J. Immunol. 2009, 182, 4865-4873. [CrossRef] [PubMed]
28. Yauch, L.E.; Prestwood, T.R.; May, M.M.; Morar, M.M.; Zellweger, R.M.; Peters, B.; Sette, A.; Shresta, S. Cd4+ T cells are not required for the induction of dengue virus-specific CD8+ T cell or antibody responses but contribute to protection after vaccination. J. Immunol. 2010, 185, 5405-5416. [CrossRef] [PubMed]
29. Zompi, S.; Santich, B.H.; Beatty, P.R.; Harris, E. Protection from secondary dengue virus infection in a mouse model reveals the role of serotype cross-reactive B and T cells. J. Immunol. 2012, 188, 404-416. [CrossRef] [PubMed]
30. Johnson, A.J.; Roehrig, J.T. New mouse model for Dengue virus vaccine testing. J. Virol. 1999, 73, 783-786. [PubMed]
31. Brewoo, J.N.; Kinney, R.M.; Powell, T.D.; Arguello, J.J.; Silengo, S.J.; Partidos, C.D.; Huang, C.Y.; Stinchcomb, D.T.; Osorio, J.E. Immunogenicity and efficacy of chimeric Dengue vaccine (Denvax) formulations in interferon-deficient AG129 mice. Vaccine 2012, 30, 1513-1520. [CrossRef] [PubMed]
32. Caine, E.A.; Partidos, C.D.; Santangelo, J.D.; Osorio, J.E. Adaptation of enterovirus 71 to adult interferon deficient mice. PLoS ONE 2013, 8, e59501. [CrossRef] [PubMed]
33. Hwa, S.H.; Lee, Y.A.; Brewoo, J.N.; Partidos, C.D.; Osorio, J.E.; Santangelo, J.D. Preclinical evaluation of the immunogenicity and safety of an inactivated enterovirus 71 candidate vaccine. PLoS Negl. Trop. Dis. 2013, 7, e2538. [CrossRef] [PubMed]
34. Gaunt, E.; Harvala, H.; Osterback, R.; Sreenu, V.B.; Thomson, E.; Waris, M.; Simmonds, P. Genetic characterization of human coxsackievirus a6 variants associated with atypical hand, foot and mouth disease: A potential role of recombination in emergence and pathogenicity. J. Gen. Virol. 2015, 96, 1067-1079. [CrossRef] [PubMed]
35. Buttery, V.W.; Kenyon, C.; Grunewald, S.; Oberste, M.S.; Nix, W.A. Notes from the field: Atypical presentations of hand, foot, and mouth disease caused by coxsackievirus A6-Minnesota, 2014. MMWR 2015, 64, 805.
36. Nishimura, Y.; Shimizu, H. Cellular receptors for human enterovirus species A. Front. Microbiol. 2012, 3, 105. [CrossRef] [PubMed]
37. Feder, H.M., Jr.; Bennett, N.; Modlin, J.F. Atypical hand, foot, and mouth disease: A vesiculobullous eruption caused by coxsackie virus A6. Lancet Infect. Dis. 2014, 14, 83-86. [CrossRef]
38. Lott, J.P.; Liu, K.; Landry, M.L.; Nix, W.A.; Oberste, M.S.; Bolognia, J.; King, B. Atypical hand-foot-and-mouth disease associated with coxsackievirus A6 infection. J. Am. Acad. Dermatol. 2013, 69, 736-741. [CrossRef] [PubMed]
39. Liu, S.L.; Pan, H.; Liu, P.; Amer, S.; Chan, T.C.; Zhan, J.; Huo, X.; Liu, Y.; Teng, Z.; Wang, L.; et al. Comparative epidemiology and virology of fatal and nonfatal cases of hand, foot and mouth disease in mainland China from 2008 to 2014. Rev. Med. Virol. 2015, 25, 115-128. [CrossRef] [PubMed]
40. Zhu, F.C.; Liang, Z.L.; Li, X.L.; Ge, H.M.; Meng, F.Y.; Mao, Q.Y.; Zhang, Y.T.; Hu, Y.M.; Zhang, Z.Y.; Li, J.X.; et al. Immunogenicity and safety of an enterovirus 71 vaccine in healthy chinese children and infants: A randomised, double-blind, placebo-controlled phase 2 clinical trial. Lancet 2013, 381, 1037-1045. [CrossRef]
41. Oberste, M.S.; Penaranda, S.; Maher, K.; Pallansch, M.A. Complete genome sequences of all members of the species human enterovirus A. J. Gen. Virol. 2004, 85, 1597-1607. [CrossRef] [PubMed]
42. Gong, M.; Zhu, H.; Zhou, J.; Yang, C.; Feng, J.; Huang, X.; Ji, G.; Xu, H.; Zhu, P. Cryo-electron microscopy study of insect cell-expressed enterovirus 71 and coxsackievirus A16 virus-like particles provides a structural basis for vaccine development. J. Virol. 2014, 88, 6444-6452. [CrossRef] [PubMed]
43. Plevka, P.; Perera, R.; Cardosa, J.; Kuhn, R.J.; Rossmann, M.G. Crystal structure of human enterovirus 71. Science 2012, 336, 1274. [CrossRef] [PubMed]
44. Ren, J.; Wang, X.; Hu, Z.; Gao, Q.; Sun, Y.; Li, X.; Porta, C.; Walter, T.S.; Gilbert, R.J.; Zhao, Y.; et al. Picornavirus uncoating intermediate captured in atomic detail. Nat. Commun. 2013, 4, 1929. [CrossRef] [PubMed]
45. Foo, D.G.; Ang, R.X.; Alonso, S.; Chow, V.T.; Quak, S.H.; Poh, C.L. Identification of immunodominant VP1 linear epitope of enterovirus 71 (EV71) using synthetic peptides for detecting human anti-EV71 IgG antibodies in western blots. Clin. Microbiol. Infect. 2008, 14, 286-288. [CrossRef] [PubMed]
46. Lim, X.F.; Jia, Q.; Khong, W.X.; Yan, B.; Premanand, B.; Alonso, S.; Chow, V.T.; Kwang, J. Characterization of an isotype-dependent monoclonal antibody against linear neutralizing epitope effective for prophylaxis of enterovirus 71 infection. PLoS ONE 2012, 7, e29751. [CrossRef] [PubMed]
47. Kiener, T.K.; Jia, Q.; Meng, T.; Chow, V.T.; Kwang, J. A novel universal neutralizing monoclonal antibody against enterovirus 71 that targets the highly conserved "knob" region of VP3 protein. PLoS Negl. Trop. Dis. 2014, 8, e2895. [CrossRef] [PubMed]
48. Shi, J.; Huang, X.; Liu, Q.; Huang, Z. Identification of conserved neutralizing linear epitopes within the VP1 protein of coxsackievirus A16. Vaccine 2013, 31, 2130-2136. [CrossRef] [PubMed]
49. Xu, L.; He, D.; Yang, L.; Li, Z.; Ye, X.; Yu, H.; Zhao, H.; Li, S.; Yuan, L.; Qian, H.; et al. A broadly cross-protective vaccine presenting the neighboring epitopes within the VP1 GH loop and VP2 EF loop of enterovirus 71. Sci. Rep. 2015, 5, 12973. [CrossRef] [PubMed]
50. Zhao, H.; Li, H.Y.; Han, J.F.; Deng, Y.Q.; Zhu, S.Y.; Li, X.F.; Yang, H.Q.; Li, Y.X.; Zhang, Y.; Qin, E.D.; et al. Novel recombinant chimeric virus-like particle is immunogenic and protective against both enterovirus 71 and coxsackievirus A16 in mice. Sci. Rep. 2015, 5, 7878. [CrossRef] [PubMed]
51. Zhang, T.; Xu, Y.; Qiao, L.;Wang, Y.;Wu, X.; Fan, D.; Peng, Q.; Xu, X. Trivalent human papillomavirus (HPV) VLP vaccine covering HPV type 58 can elicit high level of humoral immunity but also induce immune interference among component types. Vaccine 2010, 28, 3479-3487. [CrossRef] [PubMed]