5f3j Citations

Broadly neutralizing epitopes in the Plasmodium vivax vaccine candidate Duffy Binding Protein.

Proc Natl Acad Sci U S A 113 6277-82 (2016)
Cited: 59 times
EuropePMC logo PMID: 27194724

Abstract

Plasmodium vivax Duffy Binding Protein (PvDBP) is the most promising vaccine candidate for P. vivax malaria. The polymorphic nature of PvDBP induces strain-specific immune responses, however, and the epitopes of broadly neutralizing antibodies are unknown. These features hamper the rational design of potent DBP-based vaccines and necessitate the identification of globally conserved epitopes. Using X-ray crystallography, small-angle X-ray scattering, hydrogen-deuterium exchange mass spectrometry, and mutational mapping, we have defined epitopes for three inhibitory mAbs (mAbs 2D10, 2H2, and 2C6) and one noninhibitory mAb (3D10) that engage DBP. These studies expand the currently known inhibitory epitope repertoire by establishing protective motifs in subdomain three outside the receptor-binding and dimerization residues of DBP, and introduce globally conserved protective targets. All of the epitopes are highly conserved among DBP alleles. The identification of broadly conserved epitopes of inhibitory antibodies provides critical motifs that should be retained in the next generation of potent vaccines for P. vivax malaria.

Reviews - 5f3j mentioned but not cited (1)

  1. Hotspots in Plasmodium and RBC Receptor-Ligand Interactions: Key Pieces for Inhibiting Malarial Parasite Invasion. Patarroyo MA, Molina-Franky J, Gómez M, Arévalo-Pinzón G, Patarroyo ME. Int J Mol Sci 21 E4729 (2020)

Articles - 5f3j mentioned but not cited (3)

  1. Broadly neutralizing epitopes in the Plasmodium vivax vaccine candidate Duffy Binding Protein. Chen E, Salinas ND, Huang Y, Ntumngia F, Plasencia MD, Gross ML, Adams JH, Tolia NH. Proc Natl Acad Sci U S A 113 6277-6282 (2016)
  2. Structural patterns of selection and diversity for Plasmodium vivax antigens DBP and AMA1. Guy AJ, Irani V, Richards JS, Ramsland PA. Malar J 17 183 (2018)
  3. Global distribution of single amino acid polymorphisms in Plasmodium vivax Duffy-binding-like domain and implications for vaccine development efforts. Mittal P, Mishra S, Kar S, Pande V, Sinha A, Sharma A. Open Biol 10 200180 (2020)


Reviews citing this publication (12)

  1. Malaria Vaccines: Recent Advances and New Horizons. Draper SJ, Sack BK, King CR, Nielsen CM, Rayner JC, Higgins MK, Long CA, Seder RA. Cell Host Microbe 24 43-56 (2018)
  2. An overview of hydrogen deuterium exchange mass spectrometry (HDX-MS) in drug discovery. Masson GR, Jenkins ML, Burke JE. Expert Opin Drug Discov 12 981-994 (2017)
  3. Advances in Hydrogen/Deuterium Exchange Mass Spectrometry and the Pursuit of Challenging Biological Systems. James EI, Murphree TA, Vorauer C, Engen JR, Guttman M. Chem Rev 122 7562-7623 (2022)
  4. Plasmodium vivax vaccine research - we've only just begun. Tham WH, Beeson JG, Rayner JC. Int J Parasitol 47 111-118 (2017)
  5. Novel Strategies for Malaria Vaccine Design. Frimpong A, Kusi KA, Ofori MF, Ndifon W. Front Immunol 9 2769 (2018)
  6. Getting in: The structural biology of malaria invasion. Kumar H, Tolia NH. PLoS Pathog 15 e1007943 (2019)
  7. Progress towards the development of a P. vivax vaccine. De SL, Ntumngia FB, Nicholas J, Adams JH. Expert Rev Vaccines 20 97-112 (2021)
  8. Research advances in hydrogen-deuterium exchange mass spectrometry for protein epitope mapping. Sun H, Ma L, Wang L, Xiao P, Li H, Zhou M, Song D. Anal Bioanal Chem 413 2345-2359 (2021)
  9. Tracking Higher Order Protein Structure by Hydrogen-Deuterium Exchange Mass Spectrometry. Benhaim M, Lee KK, Guttman M. Protein Pept Lett 26 16-26 (2019)
  10. Plasmodium vivax Duffy Binding Protein-Based Vaccine: a Distant Dream. Kar S, Sinha A. Front Cell Infect Microbiol 12 916702 (2022)
  11. Plasmodium vivax vaccine: What is the best way to go? da Veiga GTS, Moriggi MR, Vettorazzi JF, Müller-Santos M, Albrecht L. Front Immunol 13 910236 (2022)
  12. Primate malarias as a model for cross-species parasite transmission. Voinson M, Nunn CL, Goldberg A. Elife 11 e69628 (2022)

Articles citing this publication (43)

  1. The entropic force generated by intrinsically disordered segments tunes protein function. Keul ND, Oruganty K, Schaper Bergman ET, Beattie NR, McDonald WE, Kadirvelraj R, Gross ML, Phillips RS, Harvey SC, Wood ZA. Nature 563 584-588 (2018)
  2. Human vaccination against Plasmodium vivax Duffy-binding protein induces strain-transcending antibodies. Payne RO, Silk SE, Elias SC, Milne KH, Rawlinson TA, Llewellyn D, Shakri AR, Jin J, Labbé GM, Edwards NJ, Poulton ID, Roberts R, Farid R, Jørgensen T, Alanine DG, de Cassan SC, Higgins MK, Otto TD, McCarthy JS, de Jongh WA, Nicosia A, Moyle S, Hill AV, Berrie E, Chitnis CE, Lawrie AM, Draper SJ. JCI Insight 2 93683 (2017)
  3. Rapid and iterative genome editing in the malaria parasite Plasmodium knowlesi provides new tools for P. vivax research. Mohring F, Hart MN, Rawlinson TA, Henrici R, Charleston JA, Diez Benavente E, Patel A, Hall J, Almond N, Campino S, Clark TG, Sutherland CJ, Baker DA, Draper SJ, Moon RW. Elife 8 e45829 (2019)
  4. Identification of highly-protective combinations of Plasmodium vivax recombinant proteins for vaccine development. França CT, White MT, He WQ, Hostetler JB, Brewster J, Frato G, Malhotra I, Gruszczyk J, Huon C, Lin E, Kiniboro B, Yadava A, Siba P, Galinski MR, Healer J, Chitnis C, Cowman AF, Takashima E, Tsuboi T, Tham WH, Fairhurst RM, Rayner JC, King CL, Mueller I. Elife 6 e28673 (2017)
  5. Malaria parasite CelTOS targets the inner leaflet of cell membranes for pore-dependent disruption. Jimah JR, Salinas ND, Sala-Rabanal M, Jones NG, Sibley LD, Nichols CG, Schlesinger PH, Tolia NH. Elife 5 e20621 (2016)
  6. Structural basis for neutralization of Plasmodium vivax by naturally acquired human antibodies that target DBP. Urusova D, Carias L, Huang Y, Nicolete VC, Popovici J, Roesch C, Salinas ND, Dechavanne S, Witkowski B, Ferreira MU, Adams JH, Gross ML, King CL, Tolia NH. Nat Microbiol 4 1486-1496 (2019)
  7. Structural basis for inhibition of Plasmodium vivax invasion by a broadly neutralizing vaccine-induced human antibody. Rawlinson TA, Barber NM, Mohring F, Cho JS, Kosaisavee V, Gérard SF, Alanine DGW, Labbé GM, Elias SC, Silk SE, Quinkert D, Jin J, Marshall JM, Payne RO, Minassian AM, Russell B, Rénia L, Nosten FH, Moon RW, Higgins MK, Draper SJ. Nat Microbiol 4 1497-1507 (2019)
  8. DARC extracellular domain remodeling in maturating reticulocytes explains Plasmodium vivax tropism. Ovchynnikova E, Aglialoro F, Bentlage AEH, Vidarsson G, Salinas ND, von Lindern M, Tolia NH, van den Akker E. Blood 130 1441-1444 (2017)
  9. The Presence, Persistence and Functional Properties of Plasmodium vivax Duffy Binding Protein II Antibodies Are Influenced by HLA Class II Allelic Variants. Kano FS, Souza-Silva FA, Torres LM, Lima BA, Sousa TN, Alves JR, Rocha RS, Fontes CJ, Sanchez BA, Adams JH, Brito CF, Pires DE, Ascher DB, Sell AM, Carvalho LH. PLoS Negl Trop Dis 10 e0005177 (2016)
  10. Mouse and Human Monoclonal Antibodies Protect against Infection by Multiple Genotypes of Japanese Encephalitis Virus. Fernandez E, Kose N, Edeling MA, Adhikari J, Sapparapu G, Lazarte SM, Nelson CA, Govero J, Gross ML, Fremont DH, Crowe JE, Diamond MS. mBio 9 e00008-18 (2018)
  11. Recognition of Human IgG1 by Fcγ Receptors: Structural Insights from Hydrogen-Deuterium Exchange and Fast Photochemical Oxidation of Proteins Coupled with Mass Spectrometry. Shi L, Liu T, Gross ML, Huang Y. Biochemistry 58 1074-1080 (2019)
  12. Optimizing immunization protocols to elicit broadly neutralizing antibodies. Sprenger KG, Louveau JE, Murugan PM, Chakraborty AK. Proc Natl Acad Sci U S A 117 20077-20087 (2020)
  13. An engineered vaccine of the Plasmodium vivax Duffy binding protein enhances induction of broadly neutralizing antibodies. Ntumngia FB, Pires CV, Barnes SJ, George MT, Thomson-Luque R, Kano FS, Alves JRS, Urusova D, Pereira DB, Tolia NH, King CL, Carvalho LH, Adams JH. Sci Rep 7 13779 (2017)
  14. Antibody responses to Plasmodium vivax Duffy binding and Erythrocyte binding proteins predict risk of infection and are associated with protection from clinical Malaria. He WQ, Shakri AR, Bhardwaj R, França CT, Stanisic DI, Healer J, Kiniboro B, Robinson LJ, Guillotte-Blisnick M, Huon C, Siba P, Cowman A, King CL, Tham WH, Chitnis CE, Mueller I. PLoS Negl Trop Dis 13 e0006987 (2019)
  15. High-Definition Mapping of Four Spatially Distinct Neutralizing Epitope Clusters on RiVax, a Candidate Ricin Toxin Subunit Vaccine. Toth RT, Angalakurthi SK, Van Slyke G, Vance DJ, Hickey JM, Joshi SB, Middaugh CR, Volkin DB, Weis DD, Mantis NJ. Clin Vaccine Immunol 24 e00237-17 (2017)
  16. Identification and Characterization of Functional Human Monoclonal Antibodies to Plasmodium vivax Duffy-Binding Protein. Carias LL, Dechavanne S, Nicolete VC, Sreng S, Suon S, Amaratunga C, Fairhurst RM, Dechavanne C, Barnes S, Witkowski B, Popovici J, Roesch C, Chen E, Ferreira MU, Tolia NH, Adams JH, King CL. J Immunol 202 2648-2660 (2019)
  17. Identification of an Immunogenic Broadly Inhibitory Surface Epitope of the Plasmodium vivax Duffy Binding Protein Ligand Domain. George MT, Schloegel JL, Ntumngia FB, Barnes SJ, King CL, Casey JL, Foley M, Adams JH. mSphere 4 e00194-19 (2019)
  18. Antibodies to Cryptic Epitopes in Distant Homologues Underpin a Mechanism of Heterologous Immunity between Plasmodium vivax PvDBP and Plasmodium falciparum VAR2CSA. Mitran CJ, Mena A, Gnidehou S, Banman S, Arango E, Lima BAS, Lugo H, Ganesan A, Salanti A, Mbonye AK, Ntumngia F, Barakat K, Adams JH, Kano FS, Carvalho LH, Maestre AE, Good MF, Yanow SK. mBio 10 e02343-19 (2019)
  19. Suppressing allostery in epitope mapping experiments using millisecond hydrogen / deuterium exchange mass spectrometry. Deng B, Zhu S, Macklin AM, Xu J, Lento C, Sljoka A, Wilson DJ. MAbs 9 1327-1336 (2017)
  20. Whole genome sequencing of Plasmodium vivax isolates reveals frequent sequence and structural polymorphisms in erythrocyte binding genes. Ford A, Kepple D, Abagero BR, Connors J, Pearson R, Auburn S, Getachew S, Ford C, Gunalan K, Miller LH, Janies DA, Rayner JC, Yan G, Yewhalaw D, Lo E. PLoS Negl Trop Dis 14 e0008234 (2020)
  21. Protein Footprinting and X-ray Crystallography Reveal the Interaction of PD-L1 and a Macrocyclic Peptide. Niu B, Appleby TC, Wang R, Morar M, Voight J, Villaseñor AG, Clancy S, Wise S, Belzile JP, Papalia G, Wong M, Brendza KM, Lad L, Gross ML. Biochemistry 59 541-551 (2020)
  22. Mechanistic Studies of the Kinase Domains of Class IV Lanthipeptide Synthetases. Hegemann JD, Shi L, Gross ML, van der Donk WA. ACS Chem Biol 14 1583-1592 (2019)
  23. Shed EBA-175 mediates red blood cell clustering that enhances malaria parasite growth and enables immune evasion. Paing MM, Salinas ND, Adams Y, Oksman A, Jensen AT, Goldberg DE, Tolia NH. Elife 7 e43224 (2018)
  24. Diversity pattern of Duffy binding protein sequence among Duffy-negatives and Duffy-positives in Sudan. Hoque MR, Elfaki MMA, Ahmed MA, Lee SK, Muh F, Ali Albsheer MM, Hamid MMA, Han ET. Malar J 17 297 (2018)
  25. On the Evolution and Function of Plasmodium vivax Reticulocyte Binding Surface Antigen (pvrbsa). Camargo-Ayala PA, Garzón-Ospina D, Moreno-Pérez DA, Ricaurte-Contreras LA, Noya O, Patarroyo MA. Front Genet 9 372 (2018)
  26. Dynamics of IgM and IgG responses to the next generation of engineered Duffy binding protein II immunogen: Strain-specific and strain-transcending immune responses over a nine-year period. Medeiros CMP, Moreira EUM, Pires CV, Torres LM, Guimarães LFF, Alves JRS, Lima BAS, Fontes CJF, Costa HL, Brito CFA, Sousa TN, Ntumngia FB, Adams JH, Kano FS, Carvalho LH. PLoS One 15 e0232786 (2020)
  27. Genetic diversity and neutral selection in Plasmodium vivax erythrocyte binding protein correlates with patient antigenicity. Han JH, Cho JS, Ong JJY, Park JH, Nyunt MH, Sutanto E, Trimarsanto H, Petros B, Aseffa A, Getachew S, Sriprawat K, Anstey NM, Grigg MJ, Barber BE, William T, Qi G, Liu Y, Pearson RD, Auburn S, Price RN, Nosten F, Rénia L, Russell B, Han ET. PLoS Negl Trop Dis 14 e0008202 (2020)
  28. Moderately Neutralizing Epitopes in Nonfunctional Regions Dominate the Antibody Response to Plasmodium falciparum EBA-140. Salinas ND, Paing MM, Adhikari J, Gross ML, Tolia N. Infect Immun 87 e00716-18 (2019)
  29. Naturally Acquired Antibody Response to Malaria Transmission Blocking Vaccine Candidate Pvs230 Domain 1. Tentokam BCN, Amaratunga C, Alani NAH, MacDonald NJ, Narum DL, Salinas ND, Kwan JL, Suon S, Sreng S, Pereira DB, Tolia NH, Fujiwara RT, Bueno LL, Duffy PE, Coelho CH. Front Immunol 10 2295 (2019)
  30. Estimation on local transmission of malaria by serological approach under low transmission setting in Myanmar. Nyunt MH, Soe TN, Shein T, Zaw NN, Han SS, Muh F, Lee SK, Han JH, Park JH, Ha KS, Park WS, Hong SH, Kyaw MP, Han ET. Malar J 17 6 (2018)
  31. GIP: an open-source computational pipeline for mapping genomic instability from protists to cancer cells. Späth GF, Bussotti G. Nucleic Acids Res 50 e36 (2022)
  32. Inhibition of a malaria host-pathogen interaction by a computationally designed inhibitor. Tobin AR, Crow R, Urusova DV, Klima JC, Tolia NH, Strauch EM. Protein Sci 32 e4507 (2023)
  33. Design of a stabilized non-glycosylated Pfs48/45 antigen enables a potent malaria transmission-blocking nanoparticle vaccine. Dickey TH, Gupta R, McAleese H, Ouahes T, Orr-Gonzalez S, Ma R, Muratova O, Salinas ND, Hume JCC, Lambert LE, Duffy PE, Tolia NH. NPJ Vaccines 8 20 (2023)
  34. Generation of a Peptide Vaccine Candidate against Falciparum Placental Malaria Based on a Discontinuous Epitope. Mitran CJ, Higa LM, Good MF, Yanow SK. Vaccines (Basel) 8 E392 (2020)
  35. Surveillance on the Vivax Malaria in Endemic Areas in the Republic of Korea Based on Molecular and Serological Analyses. Lee SK, Hu F, Firdaus ER, Park JH, Han JH, Lee SE, Shin HI, Cho SH, Park WS, Lu F, Han ET. Korean J Parasitol 58 609-617 (2020)
  36. Variable immunogenicity of a vivax malaria blood-stage vaccine candidate. De SL, May S, Shah K, Slawinski M, Changrob S, Xu S, Barnes SJ, Chootong P, Ntumngia FB, Adams JH. Vaccine 39 2668-2675 (2021)
  37. A conserved epitope in VAR2CSA is targeted by a cross-reactive antibody originating from Plasmodium vivax Duffy binding protein. Iyamu U, Vinals DF, Tornyigah B, Arango E, Bhat R, Adra TR, Grewal S, Martin K, Maestre A, Overduin M, Hazes B, Yanow SK. Front Cell Infect Microbiol 13 1202276 (2023)
  38. Genetic diversity and natural selection of Plasmodium vivax reticulocyte invasion genes in Ecuador. Núñez A, Ntumngia FB, Guerra Y, Adams JH, Sáenz FE. Malar J 22 225 (2023)
  39. Human monoclonal antibodies inhibit invasion of transgenic Plasmodium knowlesi expressing Plasmodium vivax Duffy binding protein. Watson QD, Carias LL, Malachin A, Redinger KR, Bosch J, Bardelli M, Baldor L, Feufack-Donfack LB, Popovici J, Moon RW, Draper SJ, Zimmerman PA, King CL. Malar J 22 369 (2023)
  40. Hydrogen-deuterium exchange mass spectrometry identifies spatially distinct antibody epitopes on domain III of the Zika virus envelope protein. Adhikari J, Zhao H, Fernandez E, Huang Y, Diamond MS, Fremont DH, Gross ML. J Mass Spectrom 56 e4685 (2021)
  41. Multiplexed Microsphere-Based Flow Cytometric Assay to Assess Strain Transcending Antibodies to Plasmodium vivax Duffy Binding Protein II Reveals an Efficient Tool to Identify Binding-Inhibitory Antibody Responders. Alves JRS, de Araújo FF, Pires CV, Teixeira-Carvalho A, Lima BAS, Torres LM, Ntumngia FB, Adams JH, Kano FS, Carvalho LH. Front Immunol 12 704653 (2021)
  42. Sequence analysis of Plasmodium vivax Duffy binding proteins reveals the presence of unique haplotypes and diversifying selection in Ethiopian isolates. Golassa L, Messele A, Oriero EC, Amambua-Ngwa A. Malar J 20 312 (2021)
  43. Structural basis for DARC binding in reticulocyte invasion by Plasmodium vivax. Moskovitz R, Pholcharee T, DonVito SM, Guloglu B, Lowe E, Mohring F, Moon RW, Higgins MK. Nat Commun 14 3637 (2023)