Immunogenicity and performance of an enterovirus 71 virus-like-particle vaccine in nonhuman primates

Vaccine

Volumn 33, Issue 44, 2015, Pages 6017-6024

  Lim, Pei Yin ^a   Hickey, Andrew C ^b,c   Jamiluddin, Mohamad F ^a   Hamid, Sharifah ^a   Kramer, Joshua ^d   Santos, Rosemary ^e   Bossart, Katharine N ^f   Cardosa, M Jane ^a  

^a Sentinext Therapeutics   (Malaysia)

^b U S PUBLIC HEALTH SERVICE   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f Integrated Research Associates   (United States)

Author keywords

Enterovirus 71; Immunogenicity; Vaccine; Virus like particles; VLP

Indexed keywords

ENTEROVIRUS 71 VIRUS LLIKE PARTICLE VACCINE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; UNCLASSIFIED DRUG; VIRUS LIKE PARTICLE VACCINE; VIRUS VACCINE; NEUTRALIZING ANTIBODY; RECOMBINANT VACCINE; VIRUS ANTIBODY;

ANTIBODY RESPONSE; ARTICLE; BIOCHEMICAL ANALYSIS; BLOOD CELL COUNT; BLOOD SAMPLING; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG DESIGN; DRUG PURIFICATION; ENTEROVIRUS 71; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOPATHOLOGY; IMMUNOGENICITY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; VACCINATION; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS LIKE AGENT; ANIMAL; BACULOVIRIDAE; BLOOD; CELL LINE; CROSS REACTION; DISEASE MODEL; ENTEROVIRUS A; ENTEROVIRUS INFECTIONS; FEMALE; GENETICS; IMMUNIZATION; IMMUNOLOGY; INSECT; ISOLATION AND PURIFICATION; PATHOLOGY; PILOT STUDY; SERODIAGNOSIS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BACULOVIRIDAE; CELL LINE; CROSS REACTIONS; DISEASE MODELS, ANIMAL; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; FEMALE; IMMUNIZATION SCHEDULE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INSECTS; MACACA MULATTA; MICE; NEUTRALIZATION TESTS; PILOT PROJECTS; VACCINES, SYNTHETIC; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84947484371     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.05.108     Document Type: Article

References (44)

1. Christian K.A., Ijaz K., Dowell S.F., Chow C.C., Chitale R.A., Bresee J.S., et al. What we are watching - five top global infectious disease threats, 2012: a perspective from CDC's Global Disease Detection Operations Center. Emerg Health Threats J 2013, 6:20632.
2. Yip C.C., Lau S.K., Woo P.C., Yuen K.Y. Human enterovirus 71 epidemics: what's next?. Emerg Health Threats J 2013, 6:19780.
3. Bossart K.N., Lee S.S., Lim P.Y., Cardosa M.J. Progress towards enterovirus 71 vaccines: conventional and novel approaches. F1000Res 2015, [in press].
4. Racaniello V.R. Picornaviridae: the viruses and their replication. Fields virology 2007, 795-838. Lippincott Williams & Wilkins, Philadelphia, PA, USA. 5th ed.
5. McMinn P., Lindsay K., Perera D., Chan H.M., Chan K.P., Cardosa M.J. Phylogenetic analysis of enterovirus 71 strains isolated during linked epidemics in Malaysia, Singapore, and Western Australia. J Virol 2001, 75(16):7732-7738.
6. Cheng A., Fung C.P., Liu C.C., Lin Y.T., Tsai H.Y., Chang S.C., et al. A phase I, randomized, open-label study to evaluate the safety and immunogenicity of an enterovirus 71 vaccine. Vaccine 2013 May 7, 31(20):2471-2476.
7. Li R., Liu L., Mo Z., Wang X., Xia J., Liang Z., et al. An inactivated enterovirus 71 vaccine in healthy children. N Engl J Med 2014, 370(9):829-837.
8. Zhu F., Xu W., Xia J., Liang Z., Liu Y., Zhang X., et al. Efficacy, safety, and immunogenicity of an enterovirus 71 vaccine in China. N Engl J Med 2014 Feb 27, 370(9):818-828.
9. Zhu F.C., Meng F.Y., Li J.X., Li X.L., Mao Q.Y., Tao 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(9882):2024-2032.
10. Li H.Y., Han J.F., Qin C.F., Chen R. Virus-like particles for enterovirus 71 produced from Saccharomyces cerevisiae potently elicits protective immune responses in mice. Vaccine 2013, 31(32):3281-3287.
11. Chung Y.C., Ho M.S., Wu J.C., Chen W.J., Huang J.H., Chou S.T., et al. Immunization with virus-like particles of enterovirus 71 elicits potent immune responses and protects mice against lethal challenge. Vaccine 2008, 26(15):1855-1862.
12. Chua B.H., Phuektes P., Sanders S.A., Nicholls P.K., McMinn P.C. The molecular basis of mouse adaptation by human enterovirus 71. J Gen Virol 2008, 89(Pt 7):1622-1632.
13. Khong W.X., Yan B., Yeo H., Tan E.L., Lee J.J., Ng J.K., et al. 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(4):2121-2131.
14. Mao Q., Dong C., Li X., Gao Q., Guo Z., Yao X., et al. Comparative analysis of the immunogenicity and protective effects of inactivated EV71 vaccines in mice. PLoS ONE 2012, 7(9):e46043.
15. 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, (March).
16. Bek E.J., Hussain K.M., Phuektes P., Kok C.C., Gao Q., Cai F., et al. Formalin-inactivated vaccine provokes cross-protective immunity in a mouse model of human enterovirus 71 infection. Vaccine 2011, 29(29-30):4829-4838.
17. Ku Z., Liu Q., Ye X., Cai Y., Wang X., Shi J., et al. A virus-like particle based bivalent vaccine confers dual protection against enterovirus 71 and coxsackievirus A16 infections in mice. Vaccine 2014, 32(34):4296-4303.
18. Hashimoto I., Hagiwara A. Pathogenicity of a poliomyelitis-like disease in monkeys infected orally with enterovirus 71: a model for human infection. Neuropathol Appl Neurobiol 1982, 8(2):149-156.
19. Chumakov M., Voroshilova M., Shindarov L., Lavrova I., Gracheva L., Koroleva G., et al. Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol 1979, 60(3-4):329-340.
20. Liu L., Zhao H., Zhang Y., Wang J., Che Y., Dong C., et al. Neonatal rhesus monkey is a potential animal model for studying pathogenesis of EV71 infection. Virology 2011, 412(1):91-100.
21. Zhang Y., Cui W., Liu L., Wang J., Zhao H., Liao Y., et al. Pathogenesis study of enterovirus 71 infection in rhesus monkeys. Lab Invest J Tech Methods Pathol 2011, 91(9):1337-1350.
22. Nagata N., Iwasaki T., Ami Y., Tano Y., Harashima A., Suzaki Y., et al. Differential localization of neurons susceptible to enterovirus 71 and poliovirus type 1 in the central nervous system of cynomolgus monkeys after intravenous inoculation. J Gen Virol 2004, 85(Pt 10):2981-2989.
23. Nagata N., Shimizu H., Ami Y., Tano Y., Harashima A., Suzaki Y., et al. Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol 2002, 67(2):207-216.
24. Hashimoto I., Hagiwara A., Kodama H. Neurovirulence in cynomolgus monkeys of enterovirus 71 isolated from a patient with hand, foot and mouth disease. Arch Virol 1978, 56(3):257-261.
25. Koroleva G.A., Karmysheva V.Y., Lukashev A.N. Enterovirus 71 pathogenicity in monkeys and cotton rats. Arch Virol 2014, 159(5):1133-1138.
26. Dong C., Liu L., Zhao H., Wang J., Liao Y., Zhang X., et al. Immunoprotection elicited by an enterovirus type 71 experimental inactivated vaccine in mice and rhesus monkeys. Vaccine 2011, 29(37):6269-6275.
27. Dong C., Wang J., Liu L., Zhao H., Shi H., Zhang Y., et al. Optimized development of a candidate strain of inactivated EV71 vaccine and analysis of its immunogenicity in rhesus monkeys. Hum Vaccines 2010, 6(12):1028-1037.
28. Lin Y.L., Yu C.I., Hu Y.C., Tsai T.J., Kuo Y.C., Chi W.K., et al. Enterovirus type 71 neutralizing antibodies in the serum of macaque monkeys immunized with EV71 virus-like particles. Vaccine 2012, 30(7):1305-1312.
29. Plevka P., Lim P.Y., Perera R., Cardosa J., Suksatu A., Kuhn R.J., et al. Neutralizing antibodies can initiate genome release from human enterovirus 71. Proc Natl Acad Sci U S A 2014, 111(6):2134-2139.
30. Hickey A.C., Koster J.A., Thalmann C.M., Hardcastle K., Tio P.H., Cardosa M.J., et al. Serotype-specific host responses in rhesus macaques after primary dengue challenge. Am J Trop Med Hyg 2013, 89(6):1043-1057.
31. Chan L.G., Parashar U.D., Lye M.S., Ong F.G., Zaki S.R., Alexander J.P., et al. Deaths of children during an outbreak of hand, foot, and mouth disease in sarawak, malaysia: clinical and pathological characteristics of the disease For the Outbreak Study Group. Clin Infect Dis 2000, 31(3):678-683.
32. Guide for the Care and Use of Laboratory Animals 2011, National Academies of Science Press, Washington, DC. 8th ed.
33. Bossart K.N., Rockx B., Feldmann F., Brining D., Scott D., LaCasse R., et al. A Hendra virus G glycoprotein subunit vaccine protects African green monkeys from Nipah virus challenge. Sci Trans Med 2012, 4(146):146ra07.
34. Yusof M.A., Rais F., Abdullah M.A., Zamri L.A., Md Ali H., Md Kassim F., et al. Molecular epidemiology of human enterovirus71 (HEV71) strains isolated in Peninsular Malaysia and Sabah from year 2001 to 2009. J Gen Mol Virol 2011, 3(1):18-26.
35. Ooi M.H., Wong S.C., Podin Y., Akin W., del Sel S., Mohan A., et al. Human enterovirus 71 disease in Sarawak Malaysia: a prospective clinical, virological, and molecular epidemiological study. Clin infect Dis 2007, 44(5):646-656.
36. Mizuta K., Abiko C., Murata T., Matsuzaki Y., Itagaki T., Sanjoh K., et al. Frequent importation of enterovirus 71 from surrounding countries into the local community of Yamagata, Japan, between 1998 and 2003. J Clin Microbiol 2005, 43(12):6171-6175.
37. Wu W.H., Kuo T.C., Lin Y.T., Huang S.W., Liu H.F., Wang J., et al. Molecular epidemiology of enterovirus 71 infection in the central region of Taiwan from 2002 to 2012. PLOS ONE 2013, 8(12):e83711.
38. AbuBakar S., Sam I.C., Yusof J., Lim M.K., Misbah S., MatRahim N., et al. Enterovirus 71 outbreak, Brunei. Emerg Infect Dis 2009, 15(1):79-82.
39. Linsuwanon P., Puenpa J., Huang S.W., Wang Y.F., Mauleekoonphairoj J., Wang J.R., et al. Epidemiology and seroepidemiology of human enterovirus 71 among Thai populations. J Biomed Sci 2014, 21:16.
40. Chan Y.F., Sam I.C., AbuBakar S. Phylogenetic designation of enterovirus 71 genotypes and subgenotypes using complete genome sequences. Infect Genet Evol 2010, 10(3):404-412.
41. Wang Y.F., Yu C.K. Animal models of enterovirus 71 infection: applications and limitations. J Biomed Sci 2014, 21:31.
42. Lin Y.W., Yu S.L., Shao H.Y., Lin H.Y., Liu C.C., Hsiao K.N., et al. Human SCARB2 transgenic mice as an infectious animal model for enterovirus 71. PLOS ONE 2013, 8(2):e57591.
43. Fujii K., Nagata N., Sato Y., Ong K.C., Wong K.T., Yamayoshi S., et al. Transgenic mouse model for the study of enterovirus 71 neuropathogenesis. Proc Natl Acad Sci U S A 2013, 110(36):14753-14758.
44. Shingler K.L., Cifuente J.O., Ashley R.E., Makhov A.M., Conway J.F., Hafenstein S. The enterovirus 71 procapsid binds neutralizing antibodies and rescues virus infection in vitro. J Virol 2015, 89(3):1900-1908.