Recombinant dengue 2 Virus NS3 helicase protein enhances antibody and T-Cell response of purified inactivated vaccine

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Simmons, Monika ^a   Sun, Peifang ^a   Putnak, Robert ^b  

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

^b WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTIBODY; GAMMA INTERFERON; HELICASE; IMMUNOGLOBULIN G; INACTIVATED VACCINE; NEUTRALIZING ANTIBODY; NONSTRUCTURAL PROTEIN 3; PROTEINASE; VIRUS ANTIGEN; NS3 PROTEIN, FLAVIVIRUS; RNA HELICASE; SERINE PROTEINASE; VIRAL PROTEIN; VIRUS ANTIBODY; VIRUS VACCINE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIBODY DEPENDENT ENHANCEMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 2; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; ESCHERICHIA COLI; FEMALE; IMMUNE RESPONSE; IMMUNOGENICITY; LYMPHOCYTE DEPLETION; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SERODIAGNOSIS; T LYMPHOCYTE; VIRUS REPLICATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; DBA MOUSE; DENGUE VIRUS; GENETIC RECOMBINATION; IMMUNOLOGY;

ANIMALS; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; DENGUE VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; INTERFERON-GAMMA; MICE; MICE, INBRED DBA; RECOMBINATION, GENETIC; RNA HELICASES; SERINE ENDOPEPTIDASES; VACCINES, INACTIVATED; VIRAL NONSTRUCTURAL PROTEINS; VIRAL VACCINES;

EID: 84962735334     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0152811     Document Type: Article

References (48)

1. Ranjit S, Kissoon N. Dengue hemorrhagic fever and shock syndromes. Pediatr Crit Care Med. 2011; 12 (1):90-100. Epub 2010/07/20. doi: 10.1097/PCC.0b013e3181e911a7 PMID: 20639791.
2. Halstead SB. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res. 2003; 60:421-67. Epub 2003/12/24. PMID: 14689700.
3. Guy B, Barrere B, Malinowski C, Saville M, Teyssou R, Lang J. From research to phase III: preclinical, industrial and clinical development of the Sanofi Pasteur tetravalent dengue vaccine. Vaccine. 2011; 29(42):7229-41. Epub 2011/07/13. doi: 10.1016/j.vaccine.2011.06.094 PMID: 21745521.
4. Coller BA, Clements DE. Dengue vaccines: progress and challenges. Curr Opin Immunol. 2011; 23 (3):391-8. Epub 2011/04/26. doi: 10.1016/j.coi.2011.03.005 PMID: 21514129.
5. Durbin AP, Whitehead SS. Next-generation dengue vaccines: novel strategies currently under development. Viruses. 2011; 3(10):1800-14. Epub 2011/11/10. doi: 10.3390/v3101800 PMID: 22069516; PubMed Central PMCID: PMC3205382.
6. Schmitz J, Roehrig J, Barrett A, Hombach J. Next generation dengue vaccines: a review of candidates in preclinical development. Vaccine. 2011; 29(42):7276-84. Epub 2011/07/26. doi: 10.1016/j.vaccine. 2011.07.017 PMID: 21781998.
7. Edelman R. Unique challenges faced by the clinical evaluation of dengue vaccines. Expert Rev Vaccines. 2011; 10(2):133-6. Epub 2011/02/22. doi: 10.1586/erv.10.159 PMID: 21332260.
8. Thomas SJ. The necessity and quandaries of dengue vaccine development. J Infect Dis. 2011; 203 (3):299-303. Epub 2011/01/07. doi: 10.1093/infdis/jiq060 PMID: 21208919; PubMed Central PMCID: PMC3071120.
9. Endy TP, Anderson KB, Nisalak A, Yoon IK, Green S, Rothman AL, et al. Determinants of inapparent and symptomatic dengue infection in a prospective study of primary school children in Kamphaeng Phet, Thailand. PLoS Negl Trop Dis. 2011; 5(3):e975. Epub 2011/03/11. doi: 10.1371/journal.pntd. 0000975 PMID: 21390158; PubMed Central PMCID: PMC3046956.
10. Kaltenbock A, Dubischar-Kastner K, Eder G, Jilg W, Klade C, Kollaritsch H, et al. Safety and immunogenicity of concomitant vaccination with the cell-culture based Japanese Encephalitis vaccine IC51 and the hepatitis A vaccine HAVRIX1440 in healthy subjects: A single-blind, randomized, controlled Phase 3 study. Vaccine. 2009; 27(33):4483-9. Epub 2009/06/03. doi: 10.1016/j.vaccine.2009.05.034 PMID: 19486955.
11. Putnak R, Barvir DA, Burrous JM, Dubois DR, D'Andrea VM, Hoke CH, et al. Development of a purified, inactivated, dengue-2 virus vaccine prototype in Vero cells: immunogenicity and protection in mice and rhesus monkeys. J Infect Dis. 1996; 174(6):1176-84. Epub 1996/12/01. PMID: 8940206.
12. Simmons M, Burgess T, Lynch J, Putnak R. Protection against dengue virus by non-replicating and live attenuated vaccines used together in a prime boost vaccination strategy. Virology. 2010; 396(2):280-8. Epub 2009/11/17. doi: 10.1016/j.virol.2009.10.023 PMID: 19913867.
13. Fernandez S, Thomas SJ, De La Barrera R, Im-Erbsin R, Jarman RG, Baras B, et al. An adjuvanted, tetravalent dengue virus purified inactivated vaccine candidate induces long-lasting and protective antibody responses against dengue challenge in rhesus macaques. Am J Trop Med Hyg. 2015; 92(4):698-708. doi: 10.4269/ajtmh.14-0268 PMID: 25646261; PubMed Central PMCID: PMC4385761.
14. Simmons M, Porter KR, Hayes CG, Vaughn DW, Putnak R. Characterization of antibody responses to combinations of a dengue virus type 2 DNA vaccine and two dengue virus type 2 protein vaccines in rhesus macaques. J Virol. 2006; 80(19):9577-85. Epub 2006/09/16. doi: 10.1128/JVI.00284-06 PMID: 16973561; PubMed Central PMCID: PMC1617260.
15. Stephenson JR. The problem with dengue. Trans R Soc Trop Med Hyg. 2005; 99(9):643-6. Epub 2005/07/05. doi: 10.1016/j.trstmh.2005.05.003 PMID: 15993908.
16. Kurane I, Dai LC, Livingston PG, Reed E, Ennis FA. Definition of an HLA-DPw2-restricted epitope on NS3, recognized by a dengue virus serotype-cross-reactive human CD4+ CD8- cytotoxic T-cell clone. J Virol. 1993; 67(10):6285-8. Epub 1993/10/01. PMID: 7690424; PubMed Central PMCID: PMC238054.
17. Falgout B, Pethel M, Zhang YM, Lai CJ. Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of dengue virus nonstructural proteins. J Virol. 1991; 65(5):2467-75. Epub 1991/ 05/01. PMID: 2016768; PubMed Central PMCID: PMC240601.
18. Falgout B, Miller RH, Lai CJ. Deletion analysis of dengue virus type 4 nonstructural protein NS2B: identification of a domain required for NS2B-NS3 protease activity. J Virol. 1993; 67(4):2034-42. Epub 1993/04/01. PMID: 8383225; PubMed Central PMCID: PMC240272.
19. Simmons CP, Dong T, Chau NV, Dung NT, Chau TN, Thao le TT, et al. Early T-cell responses to dengue virus epitopes in Vietnamese adults with secondary dengue virus infections. J Virol. 2005; 79 (9):5665-75. Epub 2005/04/14. doi: 10.1128/JVI.79.9.5665-5675.2005 PMID: 15827181; PubMed Central PMCID: PMC1082776.
20. Haller AA LG, King TH, Kemmler C, Fiolski V, Lu Y, Bellgrau D, et al. Whole recombinant yeast-based immunotherapy induces potent T cell responses targeting HCV NS3 and Core proteins. Vaccine. 2007; 25:1452-63. PMID: 17098335
21. Jiao X, Wang RY, Qiu Q, Alter HJ, Shih JW. Enhanced hepatitis C virus NS3 specific Th1 immune responses induced by co-delivery of protein antigen and CpG with cationic liposomes. J Gen Virol. 2004; 85(Pt 6):1545-53. PMID: 15166438.
22. Gao M, Wang H-P, Wang Y-N, Zhou Y, Wang Q-L. HCV-NS3 Th1 minigene vaccine based on invariant chain CLIP genetic substitution enhances CD4+ Th1 cell responses in vivo. Vaccine. 2006; 24 (26):5491-7. PMID: 16725235
23. López L, Venteo A, Jiménez-Clavero MA, Carrasco JL, Cano MJ, Soria E, et al. Evaluation of the baculovirus and E. coli-expressed non-structural (NS) proteins of bluetongue virus (BTV) as antigen in an indirect or competition ELISA to differentiate infected from vaccinated animals. Microbial Cell Factories. 2006; 5(Suppl 1):P59.
24. Wüest T, Both GW, Prince AM, Hofmann C, Löser P. Recombinant ovine atadenovirus induces a strong and sustained T cell response against the hepatitis C virus NS3 antigen in mice. Vaccine. 2004; 22 (21):2717-21.
25. Simmons M, Murphy GS, Kochel T, Raviprakash K, Hayes CG. Characterization of antibody responses to combinations of a dengue-2 DNA and dengue-2 recombinant subunit vaccine. Am J Trop Med Hyg. 2001; 65(5):420-6. Epub 2001/11/22. PMID: 11716093.
26. Russell PK, Nisalak A. Dengue virus identification by the plaque reduction neutralization test. J Immunol. 1967; 99(2):291-6. Epub 1967/08/01. PMID: 4961907.
27. Bray M, Zhao BT, Markoff L, Eckels KH, Chanock RM, Lai CJ. Mice immunized with recombinant vaccinia virus expressing dengue 4 virus structural proteins with or without nonstructural protein NS1 are protected against fatal dengue virus encephalitis. J Virol. 1989; 63(6):2853-6. Epub 1989/06/01. PMID: 2724416; PubMed Central PMCID: PMC250798.
28. Kaufman B, Summers P, Dubois D, Cohen WH, Gentry M. Monoclonal antibodies for dengue virus prM glycoprotein protect mice against lethal dengue infection. DTIC Document, 1989.
29. Falgout B, Bray M, Schlesinger JJ, Lai CJ. Immunization of mice with recombinant vaccinia virus expressing authentic dengue virus nonstructural protein NS1 protects against lethal dengue virus encephalitis. J Virol. 1990; 64(9):4356-63. Epub 1990/09/01. PMID: 2143542; PubMed Central PMCID: PMC247903.
30. Schlesinger JJ, Brandriss MW, Walsh EE. Protection of mice against dengue 2 virus encephalitis by immunization with the dengue 2 virus non-structural glycoprotein NS1. J Gen Virol. 1987; 68 (Pt 3):853-7. Epub 1987/03/01. PMID: 3819700.
31. Zhang YM, Hayes EP, McCarty TC, Dubois DR, Summers PL, Eckels KH, et al. Immunization of mice with dengue structural proteins and nonstructural protein NS1 expressed by baculovirus recombinant induces resistance to dengue virus encephalitis. J Virol. 1988; 62(8):3027-31. Epub 1988/08/01. PMID: 2969058; PubMed Central PMCID: PMC253742.
32. Mathew A, Rothman AL. Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunol Rev. 2008; 225:300-13. Epub 2008/10/08. doi: 10.1111/j.1600-065X.2008.00678.x PMID: 18837790.
33. Rothman AL. Dengue: defining protective versus pathologic immunity. J Clin Invest. 2004; 113(7):946-51. Epub 2004/04/02. doi: 10.1172/JCI21512 PMID: 15057297; PubMed Central PMCID: PMC379334.
34. Appanna R, Huat TL, See LL, Tan PL, Vadivelu J, Devi S. Cross-reactive T-cell responses to the nonstructural regions of dengue viruses among dengue fever and dengue hemorrhagic fever patients in Malaysia. Clin Vaccine Immunol. 2007; 14(8):969-77. Epub 2007/06/15. doi: 10.1128/CVI.00069-07 PMID: 17567768; PubMed Central PMCID: PMC2044482.
35. Whitehead SS, Blaney JE, Durbin AP, Murphy BR. Prospects for a dengue virus vaccine. Nat Rev Microbiol. 2007; 5(7):518-28. Epub 2007/06/15. doi: 10.1038/nrmicro1690 PMID: 17558424.
36. Spaulding AC, Kurane I, Ennis FA, Rothman AL. Analysis of murine CD8(+) T-cell clones specific for the Dengue virus NS3 protein: flavivirus cross-reactivity and influence of infecting serotype. J Virol. 1999; 73(1):398-403. Epub 1998/12/16. PMID: 9847344; PubMed Central PMCID: PMC103845.
37. Valdés K, Alvarez M, Pupo M, Vázquez S, Rodríguez R, Guzmán MG. Human dengue antibodies against structural and nonstructural proteins. Clin Diagn Lab Immunol. 2000; 7(5):856-7. PMID: 10973471
38. Churdboonchart V, Bhamarapravati N, Peampramprecha S, Sirinavin S. Antibodies against dengue viral proteins in primary and secondary dengue hemorrhagic fever. Am J Trop Med Hyg. 1991; 44 (5):481-93. Epub 1991/05/01. PMID: 2063952.
39. Konishi E, Ajiro N, Nukuzuma C, Mason PW, Kurane I. Comparison of protective efficacies of plasmid DNAs encoding Japanese encephalitis virus proteins that induce neutralizing antibody or cytotoxic T lymphocytes in mice. Vaccine. 2003; 21(25):3675-83.
40. Morozova OV, Maksimova TG, Bakhvalova VN. Tick-borne encephalitis virus NS3 gene expression does not protect mice from homologous viral challenge. Viral Immunol. 1999; 12(4):277-80. PMID: 10630787
41. Rau H, Revets H, Balmelli C, McCullough KC, Summerfield A. Immunological properties of recombinant classical swine fever virus NS3 protein in vitro and in vivo. Vet Res. 2006; 37(1):155-68. PMID: 16336932
42. Álvarez-Rodríguez LM, Ramos-Ligonio A, Rosales-Encina JL, Martínez-Cázares MT, Parissi-Crivelli A, López-Monteon A. Expression, purification, and evaluation of diagnostic potential and immunogenicity of a recombinant NS3 protein from all serotypes of dengue virus. J Trop Med. 2012;2012.
43. Ramírez R, Falcón R, Izquierdo A, García A, Alvarez M, Pérez AB, et al. Recombinant dengue 2 virus NS3 protein conserves structural antigenic and immunological properties relevant for dengue vaccine design. Virus Genes. 2014; 49(2):185-95. doi: 10.1007/s11262-014-1087-3 PMID: 24854144
44. Costa SM, Yorio AP, Goncalves A, Vidale MM, Costa E, Mohana-Borges R, et al. Induction of a protective response in mice by the dengue virus NS3 protein using DNA vaccines. PLoS One. 2011; 6(10): e25685. doi: 10.1371/journal.pone.0025685 PMID: 22031819
45. Vogelzang A, Perdomo C, Zedler U, Kuhlmann S, Hurwitz R, Gengenbacher M, et al. Central memory CD4+ T cells are responsible for the recombinant Bacillus Calmette-Guerin DeltaureC::hly vaccine's superior protection against tuberculosis. J Infect Dis. 2014; 210(12):1928-37. doi: 10.1093/infdis/jiu347 PMID: 24943726; PubMed Central PMCID: PMCPMC4241943.
46. Sitati EM, Diamond MS. CD4+ T-cell responses are required for clearance of West Nile virus from the central nervous system. J Virol. 2006; 80(24):12060-9. PMID: 17035323
47. Brien JD, Uhrlaub JL, Nikolich-Žugich J. West Nile virus-specific CD4 T cells exhibit direct antiviral cytokine secretion and cytotoxicity and are sufficient for antiviral protection. The Journal of Immunology. 2008; 181(12):8568-75. PMID: 19050276
48. Rivino L, Kumaran EA, Jovanovic V, Nadua K, Teo EW, Pang SW, et al. Differential Targeting of Viral Components by CD4+ versus CD8+ T Lymphocytes in Dengue Infection. J Virol. 2012:JVI. 02675-12.