Viral vectors for malaria vaccine development

Shengqiang Li, Emily Locke, Joseph Bruder, David Clarke, Denise L Doolan, Menzo J E Havenga, Adrian V S Hill, Peter Liljestrom, Thomas P Monath, Hussein Y Naim, Christian Ockenhouse, De-chu C Tang, Kent R Van Kampen, Jean-Francois Viret, Fidel Zavala, Filip Dubovsky, Shengqiang Li, Emily Locke, Joseph Bruder, David Clarke, Denise L Doolan, Menzo J E Havenga, Adrian V S Hill, Peter Liljestrom, Thomas P Monath, Hussein Y Naim, Christian Ockenhouse, De-chu C Tang, Kent R Van Kampen, Jean-Francois Viret, Fidel Zavala, Filip Dubovsky

Abstract

A workshop on viral vectors for malaria vaccine development, organized by the PATH Malaria Vaccine Initiative, was held in Bethesda, MD on October 20, 2005. Recent advancements in viral-vectored malaria vaccine development and emerging vector technologies were presented and discussed. Classic viral vectors such as poxvirus, adenovirus and alphavirus vectors have been successfully used to deliver malaria antigens. Some of the vaccine candidates have demonstrated their potential in inducing malaria-specific immunity in animal models and human trials. In addition, emerging viral-vector technologies, such as measles virus (MV), vesicular stomatitis virus (VSV) and yellow fever (YF) virus, may also be useful for malaria vaccine development. Studies in animal models suggest that each viral vector is unique in its ability to induce humoral and/or cellular immune responses. Those studies have also revealed that optimization of Plasmodium genes for mammalian expression is an important aspect of vaccine design. Codon-optimization, surface-trafficking, de-glycosylation and removal of toxic domains can lead to improved immunogenicity. Understanding the vector's ability to induce an immune response and the expression of malaria antigens in mammalian cells will be critical in designing the next generation of viral-vectored malaria vaccines.

References

    1. Breman J.G., Alilio M.S., Mills A. Conquering the intolerable burden of malaria: what's new, what's needed: a summary. Am J Trop Med Hyg. 2004;71(2 Suppl.):1–15.
    1. Sun P., Schwenk R., White K., Stoute J.A., Cohen J., Ballou W.R. Protective immunity induced with malaria vaccine, RTS,S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. J Immunol. 2003;171(12):6961–6967.
    1. Alonso P.L., Sacarlal J., Aponte J.J., Leach A., Macete E., Milman J. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet. 2004;364(9443):1411–1420.
    1. Alonso P.L., Sacarlal J., Aponte J.J., Leach A., Macete E., Aide P. Duration of protection with RTS,S/AS02A malaria vaccine in prevention of Plasmodium falciparum disease in Mozambican children: single-blind extended follow-up of a randomised controlled trial. Lancet. 2005;366(9502):2012–2018.
    1. Satchidanandam V., Zavala F., Moss B. Studies using a recombinant vaccinia virus expressing the circumsporozoite protein of Plasmodium berghei. Mol Biochem Parasitol. 1991;48(1):89–99.
    1. Li S., Rodrigues M., Rodriguez D., Rodriguez J.R., Esteban M., Palese P. Priming with recombinant influenza virus followed by administration of recombinant vaccinia virus induces CD8+ T-cell-mediated protective immunity against malaria. Proc Natl Acad Sci USA. 1993;90(11):5214–5218.
    1. Tine J.A., Lanar D.E., Smith D.M., Wellde B.T., Schultheiss P., Ware L.A. NYVAC-Pf7: a poxvirus-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. Infect Immun. 1996;64(9):3833–3844.
    1. Ockenhouse C.F., Sun P.F., Lanar D.E., Wellde B.T., Hall B.T., Kester K. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J Infect Dis. 1998;177(6):1664–1673.
    1. Blanchard T.J., Alcami A., Andrea P., Smith G.L. Modified vaccinia virus Ankara undergoes limited replication in human cells and lacks several immunomodulatory proteins: implications for use as a human vaccine. J Gen Virol. 1998;79(Pt. 5):1159–1167.
    1. Schneider J., Gilbert S.C., Blanchard T.J., Hanke T., Robson K.J., Hannan C.M. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat Med. 1998;4(4):397–402.
    1. McConkey S.J., Reece W.H., Moorthy V.S., Webster D., Dunachie S., Butcher G. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat Med. 2003;9(6):729–735.
    1. Webster D.P., Dunachie S., Vuola J.M., Berthoud T., Keating S., Laidlaw S.M. Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proc Natl Acad Sci USA. 2005;102(13):4836–4841.
    1. Bejon P., Andrews L., Andersen R.F., Dunachie S., Webster D., Walther M. Calculation of liver-to-blood inocula, parasite growth rates, and preerythrocytic vaccine efficacy, from serial quantitative polymerase chain reaction studies of volunteers challenged with malaria sporozoites. J Infect Dis. 2005;191(4):619–626.
    1. Moorthy V.S., Imoukhuede E.B., Keating S., Pinder M., Webster D., Skinner M.A. Phase 1 evaluation of 3 highly immunogenic prime-boost regimens, including a 12-month reboosting vaccination, for malaria vaccination in Gambian men. J Infect Dis. 2004;189(12):2213–2219.
    1. Bejon P., Mwacharo J., Kai O.K., Todryk S., Keating S., Lang T. Immunogenicity of the candidate malaria vaccines FP9 and modified vaccinia virus Ankara encoding the pre-erythrocytic antigen ME-TRAP in 1–6 year old children in a malaria endemic area. Vaccine. 2006;24(22):4709–4715.
    1. Prieur E., Gilbert S.C., Schneider J., Moore A.C., Sheu E.G., Goonetilleke N. A Plasmodium falciparum candidate vaccine based on a six-antigen polyprotein encoded by recombinant poxviruses. Proc Natl Acad Sci USA. 2004;101(1):290–295.
    1. Hutchings C.L., Gilbert S.C., Hill A.V., Moore A.C. Novel protein and poxvirus-based vaccine combinations for simultaneous induction of humoral and cell-mediated immunity. J Immunol. 2005;175(1):599–606.
    1. Liang X., Casimiro D.R., Schleif W.A., Wang F., Davies M.E., Zhang Z.Q. Vectored Gag and Env but not Tat show efficacy against simian-human immunodeficiency virus 89.6P challenge in Mamu-A*01-negative rhesus monkeys. J Virol. 2005;79(19):12321–12331.
    1. Rodrigues E.G., Zavala F., Eichinger D., Wilson J.M., Tsuji M. Single immunizing dose of recombinant adenovirus efficiently induces CD8+ T cell-mediated protective immunity against malaria. J Immunol. 1997;158(3):1268–1274.
    1. Rodrigues E.G., Zavala F., Nussenzweig R.S., Wilson J.M., Tsuji M. Efficient induction of protective anti-malaria immunity by recombinant adenovirus. Vaccine. 1998;16(19):1812–1817.
    1. Aravind L., Iyer L.M., Wellems T.E., Miller L.H. Plasmodium biology: genomic gleanings. Cell. 2003;115(7):771–785.
    1. Stowers A.W., Chen Lh L.H., Zhang Y., Kennedy M.C, Zou L., Lambert L. A recombinant vaccine expressed in the milk of transgenic mice protects Aotus monkeys from a lethal challenge with Plasmodium falciparum. Proc Natl Acad Sci USA. 2002;99(1):339–344.
    1. Giersing B., Miura K., Shimp R., Wang J., Zhou H., Orcutt A. Posttranslational modification of recombinant Plasmodium falciparum apical membrane antigen 1: impact on functional immune responses to a malaria vaccine candidate. Infect Immun. 2005;73(7):3963–3970.
    1. Yang S., Nikodem D., Davidson E.A., Gowda D.C. Glycosylation and proteolytic processing of 70 kDa C-terminal recombinant polypeptides of Plasmodium falciparum merozoite surface protein 1 expressed in mammalian cells. Glycobiology. 1999;9(12):1347–1356.
    1. Bruna-Romero O., Rocha C.D., Tsuji M., Gazzinelli R.T. Enhanced protective immunity against malaria by vaccination with a recombinant adenovirus encoding the circumsporozoite protein of Plasmodium lacking the GPI-anchoring motif. Vaccine. 2004;22(27–28):3575–3584.
    1. Barouch D.H., McKay P.F., Sumida S.M., Santra S., Jackson S.S., Gorgone D.A. Plasmid chemokines and colony-stimulating factors enhance the immunogenicity of DNA priming-viral vector boosting human immunodeficiency virus type 1 vaccines. J Virol. 2003;77(16):8729–8735.
    1. Yang Z.Y., Wyatt L.S., Kong W.P., Moodie Z., Moss B., Nabel G.J. Overcoming immunity to a viral vaccine by DNA priming before vector boosting. J Virol. 2003;77(1):799–803.
    1. Casimiro D.R., Chen L., Fu T.M., Evans R.K., Caulfield M.J., Davies M.E. Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J Virol. 2003;77(11):6305–6313.
    1. Nwanegbo E., Vardas E., Gao W., Whittle H., Sun H., Rowe D. Prevalence of neutralizing antibodies to adenoviral serotypes 5 and 35 in the adult populations of The Gambia, South Africa, and the United States. Clin Diagn Lab Immunol. 2004;11(2):351–357.
    1. Kostense S., Koudstaal W., Sprangers M., Weverling G.J., Penders G., Helmus N. Adenovirus types 5 and 35 seroprevalence in AIDS risk groups supports type 35 as a vaccine vector. Aids. 2004;18(8):1213–1216.
    1. Vogels R., Zuijdgeest D., van Rijnsoever R., Hartkoorn E., Damen I., de Bethune M.P. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J Virol. 2003;77(15):8263–8271.
    1. Lemckert A.A., Sumida S.M., Holterman L., Vogels R., Truitt D.M., Lynch D.M. Immunogenicity of heterologous prime-boost regimens involving recombinant adenovirus serotype 11 (Ad11) and Ad35 vaccine vectors in the presence of anti-ad5 immunity. J Virol. 2005;79(15):9694–9701.
    1. Seshidhar Reddy P., Ganesh S., Limbach M.P., Brann T., Pinkstaff A., Kaloss M. Development of adenovirus serotype 35 as a gene transfer vector. Virology. 2003;311(2):384–393.
    1. Gao W., Robbins P.D., Gambotto A. Human adenovirus type 35: nucleotide sequence and vector development. Gene Ther. 2003;10(23):1941–1949.
    1. Sakurai F., Mizuguchi H., Yamaguchi T., Hayakawa T. Characterization of in vitro and in vivo gene transfer properties of adenovirus serotype 35 vector. Mol Ther. 2003;8(5):813–821.
    1. Ophorst O.J., Radosevic K., Havenga M.J., Pau M.G., Holterman L., Berkhout B. Immunogenicity and protection of a recombinant human adenovirus serotype 35-based malaria vaccine against Plasmodium yoelii in mice. Infect Immun. 2006;74(1):313–320.
    1. Nanda A., Lynch D.M., Goudsmit J., Lemckert A.A., Ewald B.A., Sumida S.M. Immunogenicity of recombinant fiber-chimeric adenovirus serotype 35 vector-based vaccines in mice and rhesus monkeys. J Virol. 2005;79(22):14161–14168.
    1. Van Kampen K.R., Shi Z., Gao P., Zhang J., Foster K.W., Chen D.T. Safety and immunogenicity of adenovirus-vectored nasal and epicutaneous influenza vaccines in humans. Vaccine. 2005;23(8):1029–1036.
    1. Atkins G.J., Sheahan B.J., Liljestrom P. Manipulation of the Semliki Forest virus genome and its potential for vaccine construction. Mol Biotechnol. 1996;5(1):33–38.
    1. Tubulekas I., Berglund P., Fleeton M., Liljestrom P. Alphavirus expression vectors and their use as recombinant vaccines: a minireview. Gene. 1997;190(1):191–195.
    1. Polo J.M., Belli B.A., Driver D.A., Frolov I., Sherrill S., Hariharan M.J. Stable alphavirus packaging cell lines for Sindbis virus and Semliki Forest virus-derived vectors. Proc Natl Acad Sci USA. 1999;96(8):4598–4603.
    1. Pushko P., Parker M., Ludwig G.V., Davis N.L., Johnston R.E., Smith J.F. Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology. 1997;239(2):389–401.
    1. Tsuji M., Bergmann C.C., Takita-Sonoda Y., Murata K., Rodrigues E.G., Nussenzweig R.S. Recombinant Sindbis viruses expressing a cytotoxic T-lymphocyte epitope of a malaria parasite or of influenza virus elicit protection against the corresponding pathogen in mice. J Virol. 1998;72(8):6907–6910.
    1. Chen Q., Pettersson F., Vogt A.M., Schmidt B., Ahuja S., Liljestrom P. Immunization with PfEMP1-DBL1alpha generates antibodies that disrupt rosettes and protect against the sequestration of Plasmodium falciparum-infected erythrocytes. Vaccine. 2004;22(21–22):2701–2712.
    1. Sundback M., Douagi I., Dayaraj C., Forsell M.N., Nordstrom E.K., McInerney G.M. Efficient expansion of HIV-1-specific T cell responses by homologous immunization with recombinant Semliki Forest virus particles. Virology. 2005;341(2):190–202.
    1. Nordstrom E.K., Forsell M.N., Barnfield C., Bonin E., Hanke T., Sundstrom M. Enhanced immunogenicity using an alphavirus replicon DNA vaccine against human immunodeficiency virus type 1. J Gen Virol. 2005;86(Pt. 2):349–354.
    1. Wherry E.J., Teichgraber V., Becker T.C., Masopust D., Kaech S.M., Antia R. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol. 2003;4(3):225–234.
    1. Morrot A., Hafalla J.C., Cockburn I.A., Carvalho L.H., Zavala F. IL-4 receptor expression on CD8+ T cells is required for the development of protective memory responses against liver stages of malaria parasites. J Exp Med. 2005;202(4):551–560.
    1. International Travel and Health: Vaccination Requirements and Health Advice. World Health Organization, Geneva, 1996.
    1. Poland J.D., Calisher C.H., Monath T.P., Downs W.G., Murphy K. Persistence of neutralizing antibody 30–35 years after immunization with 17D yellow fever vaccine. Bull World Health Organ. 1981;59(6):895–900.
    1. Monath T.P., Guirakhoo F., Nichols R., Yoksan S., Schrader R., Murphy C. Chimeric live, attenuated vaccine against Japanese encephalitis (ChimeriVax-JE): phase 2 clinical trials for safety and immunogenicity, effect of vaccine dose and schedule, and memory response to challenge with inactivated Japanese encephalitis antigen. J Infect Dis. 2003;188(8):1213–1230.
    1. Arroyo J., Miller C., Catalan J., Myers G.A., Ratterree M.S., Trent D.W. ChimeriVax-West Nile virus live-attenuated vaccine: preclinical evaluation of safety, immunogenicity, and efficacy. J Virol. 2004;78(22):12497–12507.
    1. Brandler S., Brown N., Ermak T.H., Mitchell F., Parsons M., Zhang Z. Replication of chimeric yellow fever virus-dengue serotype 1-4 virus vaccine strains in dendritic and hepatic cells. Am J Trop Med Hyg. 2005;72(1):74–81.
    1. Lai C.J., Monath T.P. Chimeric flaviviruses: novel vaccines against dengue fever, tick-borne encephalitis, and Japanese encephalitis. Adv Virus Res. 2003;61:469–509.
    1. Tao D., Barba-Spaeth G., Rai U., Nussenzweig V., Rice C.M., Nussenzweig R.S. Yellow fever 17D as a vaccine vector for microbial CTL epitopes: protection in a rodent malaria model. J Exp Med. 2005;201(2):201–209.
    1. Bonaldo M.C., Garratt R.C., Caufour P.S., Freire M.S., Rodrigues M.M., Nussenzweig R.S. Surface expression of an immunodominant malaria protein B cell epitope by yellow fever virus. J Mol Biol. 2002;315(4):873–885.
    1. Radecke F., Spielhofer P., Schneider H., Kaelin K., Huber M., Dotsch C. Rescue of measles viruses from cloned DNA. EMBO J. 1995;14(23):5773–5784.
    1. Lorin C., Mollet L., Delebecque F., Combredet C., Hurtrel B., Charneau P. A single injection of recombinant measles virus vaccines expressing human immunodeficiency virus (HIV) type 1 clade B envelope glycoproteins induces neutralizing antibodies and cellular immune responses to HIV. J Virol. 2004;78(1):146–157.
    1. Singh M., Cattaneo R., Billeter M.A. A recombinant measles virus expressing hepatitis B virus surface antigen induces humoral immune responses in genetically modified mice. J Virol. 1999;73(6):4823–4828.
    1. Wang Z., Hangartner L., Cornu T.I., Martin L.R., Zuniga A., Billeter M.A. Recombinant measles viruses expressing heterologous antigens of mumps and simian immunodeficiency viruses. Vaccine. 2001;19(17–19):2329–2336.
    1. Despres P., Combredet C., Frenkiel M.P., Lorin C., Brahic M., Tangy F. Live measles vaccine expressing the secreted form of the West Nile virus envelope glycoprotein protects against West Nile virus encephalitis. J Infect Dis. 2005;191(2):207–214.
    1. Fehr T., Naim H.Y., Bachmann M.F., Ochsenbein A.F., Spielhofer P., Bucher E. T-cell independent IgM and enduring protective IgG antibodies induced by chimeric measles viruses. Nat Med. 1998;4(8):945–948.
    1. Tangy F., Naim H.Y. Live attenuated measles vaccine as a potential multivalent pediatric vaccination vector. Viral Immunol. 2005;18(2):317–326.
    1. Dilraj A., Cutts F.T., de Castro J.F., Wheeler J.G., Brown D., Roth C. Response to different measles vaccine strains given by aerosol and subcutaneous routes to schoolchildren: a randomised trial. Lancet. 2000;355(9206):798–803.
    1. Wong-Chew R.M., Islas-Romero R., Garcia-Garcia Mde L., Beeler J.A., Audet S., Santos-Preciado J.I. Immunogenicity of aerosol measles vaccine given as the primary measles immunization to nine-month-old Mexican children. Vaccine. 2006;24(5):683–690.
    1. Rose N.F., Marx P.A., Luckay A., Nixon D.F., Moretto W.J., Donahoe S.M. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell. 2001;106(5):539–549.

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