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ORIGINAL RESEARCH

The αTSR Domain of Plasmodium Circumsporozoite Protein Bound Heparan Sulfates and Elicited High Titers of Sporozoite Binding Antibody After Displayed by Nanoparticles

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Pages 3087-3107 | Received 29 Jan 2023, Accepted 31 May 2023, Published online: 08 Jun 2023

References

  • World Health Organization. World Malaria Report 2021. World Health Organization; 2022.
  • World Health Organization. World Malaria Report 2019. World Health Organization; 2019.
  • Kappe SH, Buscaglia CA, Nussenzweig V. Plasmodium sporozoite molecular cell biology. Annu Rev Cell Dev Biol. 2004;20:29–59. doi:10.1146/annurev.cellbio.20.011603.150935
  • Menard R. The journey of the malaria sporozoite through its hosts: two parasite proteins lead the way. Microbes Infect. 2000;2(6):633–642. doi:10.1016/S1286-4579(00)00362-2
  • Gosling R, von Seidlein L. The Future of the RTS, S/AS01 malaria vaccine: an alternative development plan. PLoS Med. 2016;13(4):e1001994. doi:10.1371/journal.pmed.1001994
  • Laurens MB. RTS, S/AS01 vaccine (Mosquirix): an overview. Hum Vaccin Immunother. 2020;16(3):480–489. doi:10.1080/21645515.2019.1669415
  • Prudencio M, Rodriguez A, Mota MM. The silent path to thousands of merozoites: the Plasmodium liver stage. Nat Rev Microbiol. 2006;4(11):849–856. doi:10.1038/nrmicro1529
  • Sturm A, Amino R, van de Sand C, et al. Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science. 2006;313(5791):1287–1290. doi:10.1126/science.1129720
  • Gerald N, Mahajan B, Kumar S. Mitosis in the human malaria parasite Plasmodium falciparum. Eukaryotic Cell. 2011;10(4):474–482. doi:10.1128/EC.00314-10
  • Josling GA, Llinas M. Sexual development in Plasmodium parasites: knowing when it’s time to commit. Nat Rev Microbiol. 2015;13(9):573–587.
  • Bancells C, Llora-Batlle O, Poran A, et al. Revisiting the initial steps of sexual development in the malaria parasite Plasmodium falciparum. Nat Microbiol. 2019;4(1):144–154. doi:10.1038/s41564-018-0291-7
  • Bennink S, Kiesow MJ, Pradel G. The development of malaria parasites in the mosquito midgut. Cell Microbiol. 2016;18(7):905–918. doi:10.1111/cmi.12604
  • Medica DL, Sinnis P. Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infect Immun. 2005;73(7):4363–4369. doi:10.1128/IAI.73.7.4363-4369.2005
  • Sinnis P, Zavala F. The skin: where malaria infection and the host immune response begin. Semin Immunopathol. 2012;34(6):787–792. doi:10.1007/s00281-012-0345-5
  • Dundas K, Shears MJ, Sinnis P, Wright GJ. Important extracellular interactions between plasmodium sporozoites and host cells required for infection. Trends Parasitol. 2019;35(2):129–139. doi:10.1016/j.pt.2018.11.008
  • Doud MB, Koksal AC, Mi LZ, Song G, Lu C, Springer TA. Unexpected fold in the circumsporozoite protein target of malaria vaccines. Proc Natl Acad Sci USA. 2012;109(20):7817–7822. doi:10.1073/pnas.1205737109
  • Wang Q, Fujioka H, Nussenzweig V. Mutational analysis of the GPI-anchor addition sequence from the circumsporozoite protein of Plasmodium. Cell Microbiol. 2005;7(11):1616–1626. doi:10.1111/j.1462-5822.2005.00579.x
  • Pinzon-Ortiz C, Friedman J, Esko J, Sinnis P. The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for plasmodium sporozoite attachment to target cells. J Biol Chem. 2001;276(29):26784–26791. doi:10.1074/jbc.M104038200
  • Coppi A, Tewari R, Bishop JR, et al. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2007;2(5):316–327. doi:10.1016/j.chom.2007.10.002
  • Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med. 1993;177(5):1287–1298. doi:10.1084/jem.177.5.1287
  • Cerami C, Kwakye-Berko F, Nussenzweig V. Binding of malarial circumsporozoite protein to sulfatides [Gal(3-SO4)beta 1-Cer] and cholesterol-3-sulfate and its dependence on disulfide bond formation between cysteines in region II. Mol Biochem Parasitol. 1992;54(1):1–12. doi:10.1016/0166-6851(92)90089-3
  • Cerami C, Frevert U, Sinnis P, et al. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell. 1992;70(6):1021–1033. doi:10.1016/0092-8674(92)90251-7
  • Sinnis P, Clavijo P, Fenyo D, Chait BT, Cerami C, Nussenzweig V. Structural and functional properties of region II-plus of the malaria circumsporozoite protein. J Exp Med. 1994;180(1):297–306. doi:10.1084/jem.180.1.297
  • Ancsin JB, Kisilevsky R. A binding site for highly sulfated heparan sulfate is identified in the N terminus of the circumsporozoite protein: significance for malarial sporozoite attachment to hepatocytes. J Biol Chem. 2004;279(21):21824–21832. doi:10.1074/jbc.M401979200
  • Kumar KA, Sano G, Boscardin S, et al. The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature. 2006;444(7121):937–940. doi:10.1038/nature05361
  • Nussenzweig RS, Vanderberg J, Most H, Orton C. Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature. 1967;216(5111):160–162. doi:10.1038/216160a0
  • Gwadz RW, Cochrane AH, Nussenzweig V, Nussenzweig RS. Preliminary studies on vaccination of rhesus monkeys with irradiated sporozoites of Plasmodium knowlesi and characterization of surface antigens of these parasites. Bull World Health Organ. 1979;57(1):165–173.
  • Clyde DF, McCarthy VC, Miller RM, Hornick RB. Specificity of protection of man immunized against sporozoite-induced falciparum malaria. Am J Med Sci. 1973;266(6):398–403. doi:10.1097/00000441-197312000-00001
  • Romero P, Maryanski JL, Corradin G, Nussenzweig RS, Nussenzweig V, Zavala F. Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature. 1989;341(6240):323–326. doi:10.1038/341323a0
  • Reece WH, Pinder M, Gothard PK, et al. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat Med. 2004;10(4):406–410. doi:10.1038/nm1009
  • Rts SCTP. Efficacy and safety of RTS, S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a Phase 3, individually randomised, controlled trial. Lancet. 2015;386(9988):31–45.
  • Targett G. Phase 3 trial with the RTS, S/AS01 malaria vaccine shows protection against clinical and severe malaria in infants and children in Africa. Evid Based Med. 2015;20(1):9. doi:10.1136/ebmed-2014-110089
  • Tan M, Jiang X. Norovirus capsid protein-derived nanoparticles and polymers as versatile platforms for antigen presentation and vaccine development. Pharmaceutics. 2019;11(9). doi:10.3390/pharmaceutics11090472
  • Xia M, Huang P, Sun C, et al. Bioengineered norovirus S60 nanoparticles as a multifunctional vaccine platform. ACS Nano. 2018;12(11):10665–10682. doi:10.1021/acsnano.8b02776
  • Xia M, Hoq MR, Huang P, Jiang W, Jiang X, Tan M. Bioengineered pseudovirus nanoparticles displaying the HA1 antigens of influenza viruses for enhanced immunogenicity. Nano Res. 2022;2022:1–10.
  • Cibulskis RE, Alonso P, Aponte J, et al. Malaria: global progress 2000–2015 and future challenges. Infect Dis Poverty. 2016;5(1):61. doi:10.1186/s40249-016-0151-8
  • Tan M, Jiang X. The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol. 2005;79(22):14017–14030. doi:10.1128/JVI.79.22.14017-14030.2005
  • Tan M, Hegde RS, Jiang X. The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J Virol. 2004;78(12):6233–6242. doi:10.1128/JVI.78.12.6233-6242.2004
  • Wang L, Huang P, Fang H, et al. Polyvalent complexes for vaccine development. Biomaterials. 2013;34(18):4480–4492. doi:10.1016/j.biomaterials.2013.02.041
  • Xia M, Huang P, Jiang X, Tan M. A nanoparticle-based trivalent vaccine targeting the glycan binding VP8* domains of rotaviruses. Viruses. 2021;13(1):72. doi:10.3390/v13010072
  • Huang P, Farkas T, Zhong W, et al. Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns. J Virol. 2005;79(11):6714–6722. doi:10.1128/JVI.79.11.6714-6722.2005
  • Kimanius D, Dong L, Sharov G, Nakane T, Scheres SHW. New tools for automated cryo-EM single-particle analysis in RELION-4.0. Biochem J. 2021;478(24):4169–4185. doi:10.1042/BCJ20210708
  • Sun C, Gonzalez B, Vago FS, Jiang W. High resolution single particle Cryo-EM refinement using JSPR. Prog Biophys Mol Biol. 2021;160:37–42. doi:10.1016/j.pbiomolbio.2020.05.006
  • Guo F, Jiang W. Single particle cryo-electron microscopy and 3-D reconstruction of viruses. Methods Mol Biol. 2014;1117:401–443.
  • Goddard TD, Huang CC, Ferrin TE. Visualizing density maps with UCSF Chimera. J Struct Biol. 2007;157(1):281–287. doi:10.1016/j.jsb.2006.06.010
  • Burmeister WP, Buisson M, Estrozi LF, et al. Structure determination of feline calicivirus virus-like particles in the context of a pseudo-octahedral arrangement. PLoS One. 2015;10(3):e0119289. doi:10.1371/journal.pone.0119289
  • Marty MT, Baldwin AJ, Marklund EG, Hochberg GK, Benesch JL, Robinson CV. Bayesian deconvolution of mass and ion mobility spectra: from binary interactions to polydisperse ensembles. Anal Chem. 2015;87(8):4370–4376. doi:10.1021/acs.analchem.5b00140
  • Kitova EN, El-Hawiet A, Schnier PD, Klassen JS. Reliable determinations of protein-ligand interactions by direct ESI-MS measurements. Are we there yet? J Am Soc Mass Spectrom. 2012;23(3):431–441. doi:10.1007/s13361-011-0311-9
  • Sonn-Segev A, Belacic K, Bodrug T, et al. Quantifying the heterogeneity of macromolecular machines by mass photometry. Nat Commun. 2020;11(1):1772. doi:10.1038/s41467-020-15642-w
  • Tan M, Huang P, Xia M, et al. Norovirus P particle, a novel platform for vaccine development and antibody production. J Virol. 2011;85(2):753–764. doi:10.1128/JVI.01835-10
  • Xia M, Wei C, Wang L, et al. Development and evaluation of two subunit vaccine candidates containing antigens of hepatitis E virus, rotavirus, and astrovirus. Sci Rep. 2016;6:25735. doi:10.1038/srep25735
  • Xia M, Wei C, Wang L, et al. A trivalent vaccine candidate against hepatitis E virus, norovirus, and astrovirus. Vaccine. 2016;34(7):905–913. doi:10.1016/j.vaccine.2015.12.068
  • Zhang M, Mandraju R, Rai U, Shiratsuchi T, Tsuji M. Monoclonal antibodies against plasmodium falciparum circumsporozoite protein. Antibodies. 2017;6(3). doi:10.3390/antib6030011
  • Swearingen KE, Lindner SE, Shi L, et al. Interrogating the plasmodium sporozoite surface: identification of surface-exposed proteins and demonstration of glycosylation on CSP and TRAP by mass spectrometry-based proteomics. PLoS Pathog. 2016;12(4):e1005606. doi:10.1371/journal.ppat.1005606
  • Huang P, Xia M, Tan M, et al. Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J Virol. 2012;86(9):4833–4843. doi:10.1128/JVI.05507-11
  • Liu Y, Huang P, Jiang B, Tan M, Morrow AL, Jiang X. Poly-LacNAc as an age-specific ligand for rotavirus P[11] in neonates and infants. PLoS One. 2013;8(11):e78113. doi:10.1371/journal.pone.0078113
  • Liu Y, Ramelot TA, Huang P, et al. Glycan specificity of P[19] rotavirus and comparison with those of related P genotypes. J Virol. 2016;90(21):9983–9996. doi:10.1128/JVI.01494-16
  • Liu Y, Xu S, Woodruff AL, et al. Structural basis of glycan specificity of P[19] VP8*: implications for rotavirus zoonosis and evolution. PLoS Pathog. 2017;13(11):e1006707. doi:10.1371/journal.ppat.1006707
  • Tan M, Jiang X. Recent advancements in combination subunit vaccine development. Hum Vaccin Immunother. 2017;13(1):180–185. doi:10.1080/21645515.2016.1229719
  • Tan M, Jiang X. Nanoparticles of Norovirus. In: Khudyakov Y, Pumpens P, editors. Viral Nanotechnology. Norwich, UK: CRC Press, Taylor &Francis Group; 2015:363–371.
  • Tan M, Jiang X. Subviral particle as vaccine and vaccine platform. Curr Opin Virol. 2014;6:24–33. doi:10.1016/j.coviro.2014.02.009
  • Liu C, Huang P, Zhao D, et al. Effects of rotavirus NSP4 protein on the immune response and protection of the SR69A-VP8* nanoparticle rotavirus vaccine. Vaccine. 2020;2020:1.
  • Xu S, Ahmed LU, Stuckert MR, et al. Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens. PLoS Pathog. 2020;16(3):e1008386. doi:10.1371/journal.ppat.1008386
  • Xu S, McGinnis KR, Liu Y, et al. Structural basis of P[II] rotavirus evolution and host ranges under selection of histo-blood group antigens. Proc Natl Acad Sci USA. 2021;118:36.
  • Xia M, Huang P, Jiang X, Tan M. Immune response and protective efficacy of the S particle presented rotavirus VP8* vaccine in mice. Vaccine. 2019;37(30):4103–4110. doi:10.1016/j.vaccine.2019.05.075
  • Xia M, Huang P, Tan M. A pseudovirus nanoparticle-based trivalent rotavirus vaccine candidate elicits high and cross P type immune response. Pharmaceutics. 2022;14(8):1597. doi:10.3390/pharmaceutics14081597