A public antibody lineage that potently inhibits malaria infection through dual binding to the circumsporozoite protein

  • 1.

    World Health Organization. World malaria report 2016. (World Health Organization, 2017).

  • 2.

    Hoffman, S.L. et al. Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science 237, 639–642 (1987).

  • 3.

    Tran, T.M. et al. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin. Infect. Dis. 57, 40–47 (2013).

  • 4.

    Casares, S., Brumeanu, T.-D. & Richie, T.L. The RTS,S malaria vaccine. Vaccine 28, 4880–4894 (2010).

  • 5.

    Dups, J.N., Pepper, M. & Cockburn, I.A. Antibody and B cell responses to Plasmodium sporozoites. Front. Microbiol. 5, 625 (2014).

  • 6.

    Ishizuka, A.S. et al. Protection against malaria at 1 year and immune correlates following PfSPZ vaccination. Nat. Med. 22, 614–623 (2016).

  • 7.

    Cerami, C. et al. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70, 1021–1033 (1992).

  • 8.

    Frevert, U. et al. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J. Exp. Med. 177, 1287–1298 (1993).

  • 9.

    Coppi, A., Pinzon-Ortiz, C., Hutter, C. & Sinnis, P. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J. Exp. Med. 201, 27–33 (2005).

  • 10.

    RTS,S Clinical Trials Partnership. 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 386, 31–45 (2015).

  • 11.

    Coppi, A. et al. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe 2, 316–327 (2007).

  • 12.

    Coppi, A. et al. The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito to mammalian host. J. Exp. Med. 208, 341–356 (2011).

  • 13.

    Olotu, A. et al. Four-year efficacy of RTS,S/AS01E and its interaction with malaria exposure. N. Engl. J. Med. 368, 1111–1120 (2013).

  • 14.

    Olotu, A. et al. Seven-year efficacy of RTS,S/AS01 malaria vaccine among young African children. N. Engl. J. Med. 374, 2519–2529 (2016).

  • 15.

    Nussenzweig, R.S., Vanderberg, J., Most, H. & Orton, C. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 216, 160–162 (1967).

  • 16.

    Clyde, D.F., Most, H., McCarthy, V.C. & Vanderberg, J.P. Immunization of man against sporozite-induced falciparum malaria. Am. J. Med. Sci. 266, 169–177 (1973).

  • 17.

    Rieckmann, K.H., Carson, P.E., Beaudoin, R.L., Cassells, J.S. & Sell, K.W. Letter: sporozoite induced immunity in man against an Ethiopian strain of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 68, 258–259 (1974).

  • 18.

    Hoffman, S.L. et al. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185, 1155–1164 (2002).

  • 19.

    Hoffman, S.L. et al. Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum. Vaccin. 6, 97–106 (2010).

  • 20.

    Seder, R.A. et al. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341, 1359–1365 (2013).

  • 21.

    Mordmüller, B. et al. Sterile protection against human malaria by chemoattenuated PfSPZ vaccine. Nature 542, 445–449 (2017).

  • 22.

    Sissoko, M.S. et al. Safety and efficacy of PfSPZ Vaccine against Plasmodium falciparum via direct venous inoculation in healthy malaria-exposed adults in Mali: a randomised, double-blind phase 1 trial. Lancet Infect. Dis. 17, 498–509 (2017).

  • 23.

    Zavala, F. et al. Rationale for development of a synthetic vaccine against Plasmodium falciparum malaria. Science 228, 1436–1440 (1985).

  • 24.

    Kumar, K.A. et al. The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature 444, 937–940 (2006).

  • 25.

    Triller, G. et al. Natural parasite exposure induces protective human anti-malarial antibodies. Immunity 47, 1197–1209.e10 (2017).

  • 26.

    Dyson, H.J., Satterthwait, A.C., Lerner, R.A. & Wright, P.E. Conformational preferences of synthetic peptides derived from the immunodominant site of the circumsporozoite protein of Plasmodium falciparum by 1H NMR. Biochemistry 29, 7828–7837 (1990).

  • 27.

    Ghasparian, A., Moehle, K., Linden, A. & Robinson, J.A. Crystal structure of an NPNA-repeat motif from the circumsporozoite protein of the malaria parasite Plasmodium falciparum. Chem. Commun. (Camb.) 365, 174–176 (2006).

  • 28.

    Oyen, D. et al. Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein. Proc. Natl. Acad. Sci. USA 114, E10438–E10445 (2017).

  • 29.

    Fisher, C.R. et al. T-dependent B cell responses to Plasmodium induce antibodies that form a high-avidity multivalent complex with the circumsporozoite protein. PLoS Pathog. 13, e1006469 (2017).

  • 30.

    Hernández, E.C., Suárez, C.F., Parra, C.A., Patarroyo, M.A. & Patarroyo, M.E. Identification of five different IGHV gene families in owl monkeys (Aotus nancymaae). Tissue Antigens 66, 640–649 (2005).

  • 31.

    Krishnamurty, A.T. et al. Somatically hypermutated Plasmodium-specific IgM+ memory B cells are rapid, plastic, early responders upon malaria rechallenge. Immunity 45, 402–414 (2016).

  • 32.

    Weill, J.-C., Weller, S. & Reynaud, C.-A. Human marginal zone B cells. Annu. Rev. Immunol. 27, 267–285 (2009).

  • 33.

    Lindne
    r, S.E.
    et al. Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol. Cell. Proteomics 12, 1127–1143 (2013).

  • 34.

    Swearingen, K.E. 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. 12, e1005606 (2016).

  • 35.

    Rathore, D. et al. An immunologically cryptic epitope of Plasmodium falciparum circumsporozoite protein facilitates liver cell recognition and induces protective antibodies that block liver cell invasion. J. Biol. Chem. 280, 20524–20529 (2005).

  • 36.

    Bongfen, S.E. et al. The N-terminal domain of Plasmodium falciparum circumsporozoite protein represents a target of protective immunity. Vaccine 27, 328–335 (2009).

  • 37.

    Espinosa, D.A. et al. Proteolytic cleavage of the Plasmodium falciparum circumsporozoite protein is a target of protective antibodies. J. Infect. Dis. 212, 1111–1119 (2015).

  • 38.

    Tissot, A.C. et al. Versatile virus-like particle carrier for epitope based vaccines. PLoS One 5, e9809 (2010).

  • 39.

    Hsia, Y. et al. Corrigendum: Design of a hyperstable 60-subuni 60-subunit protein icosahedron. Nature 540, 150 (2016).

  • 40.

    Pappas, L. et al. Rapid development of broadly influenza neutralizing antibodies through redundant mutations. Nature 516, 418–422 (2014).

  • 41.

    Joyce, M.G. et al. Vaccine-induced antibodies that neutralize group 1 and group 2 influenza A viruses. Cell 166, 609–623 (2016).

  • 42.

    Charoenvit, Y. et al. Monoclonal, but not polyclonal, antibodies protect against Plasmodium yoelii sporozoites. J. Immunol. 146, 1020–1025 (1991).

  • 43.

    Charoenvit, Y. et al. Inability of malaria vaccine to induce antibodies to a protective epitope within its sequence. Science 251, 668–671 (1991).

  • 44.

    Sack, B.K. et al. Humoral protection against mosquito bite-transmitted Plasmodium falciparum infection in humanized mice. NPJ Vaccines 2, 27 (2017).

  • 45.

    Roggero, M.A. et al. Synthesis and immunological characterization of 104-mer and 102-mer peptides corresponding to the N- and C-terminal regions of the Plasmodium falciparum CS protein. Mol. Immunol. 32, 1301–1309 (1995).

  • 46.

    Tan, J. et al. A LAIR1 insertion generates broadly reactive antibodies against malaria variant antigens. Nature 529, 105–109 (2016).

  • 47.

    Traggiai, E. et al. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 10, 871–875 (2004).

  • 48.

    Kaushansky, A., Rezakhani, N., Mann, H. & Kappe, S.H.I. Development of a quantitative flow cytometry–based assay to assess infection by Plasmodium falciparum sporozoites. Mol. Biochem. Parasitol. 183, 100–103 (2012).

  • 49.

    Tiller, T. et al. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329, 112–124 (2008).

  • 50.

    Lefranc, M.-P. et al. IMGT, the international immunog
    enetics information system
    . Nucleic Acids Res. 37, D1006–D1012 (2009).

  • 51.

    Goujon, M. et al. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38, W695–9 (2010).

  • 52.

    Kepler, T.B. Reconstructing a B-cell clonal lineage. I. Statistical inference of unobserved ancestors. F1000Res. 2, 103 (2013).

  • 53.

    Liao, H.-X. et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496, 469–476 (2013).

  • 54.

    Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997).

  • 55.

    McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).

  • 56.

    Biasini, M. et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252–8 (2014).

  • 57.

    Bordoli, L. et al. Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4, 1–13 (2009).

  • 58.

    Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195–201 (2006).

  • 59.

    Lepore, R., Olimpieri, P.P., Messih, M.A. & Tramontano, A. PIGSPro: prediction of immunoglobulin structures v2. Nucleic Acids Res. 45 W1, W17–W23 (2017).

  • 60.

    Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213–221 (2010).

  • 61.

    Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).

  • 62.

    Connolly, M.L. The molecular surface package. J. Mol. Graph. 11, 139–141 (1993).

  • 63.

    Gelin, B.R. & Karplus, M. Side-chain torsional potentials: effect of dipeptide, protein, and solvent environment. Biochemistry 18, 1256–1268 (1979).

  • 64.

    Chen, V.B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12–21 (2010).

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