Human monoclonal antibodies inhibit invasion of transgenic Plasmodium knowlesi expressing Plasmodium vivax Duffy binding protein
Battle KE, Lucas TCD, Nguyen M, Howes RE, Nandi AK, Twohig KA, et al. Mapping the global endemicity and clinical burden of Plasmodium vivax, 2000–17: a spatial and temporal modelling study. Lancet. 2019;394:332–43.
Google Scholar
Dini S, Douglas NM, Poespoprodjo JR, Kenangalem E, Sugiarto P, Plumb ID, et al. The risk of morbidity and mortality following recurrent malaria in Papua, Indonesia: a retrospective cohort study. BMC Med. 2020;18:28.
Google Scholar
Moreira CM, Abo-Shehada M, Price RN, Drakeley CJ. A systematic review of sub-microscopic Plasmodium vivax infection. Malar J. 2015;14:360.
Google Scholar
Howes RE, Reiner RC Jr, Battle KE, Longbottom J, Mappin B, Ordanovich D, et al. Plasmodium vivax transmission in Africa. PLoS Negl Trop Dis. 2015;9: e0004222.
Google Scholar
Twohig KA, Pfeffer DA, Baird JK, Price RN, Zimmerman PA, Hay SI, et al. Growing evidence of Plasmodium vivax across malaria-endemic Africa. PLoS Negl Trop Dis. 2019;13: e0007140.
Google Scholar
Zimmerman PA. Plasmodium vivax Infection in Duffy-Negative people in Africa. Am J Trop Med Hyg. 2017;97:636–8.
Google Scholar
WHO. The potential impact of health service disruptions on the burden of malaria: a modelling analysis for countries in sub-Saharan Africa. Geneva: World Health Organization; 2020.
WHO. A year without precedent: WHO’s COVID-19 response. Geneva: World Health Organization; 2020.
WHO. World Malaria Report 2022. Geneva: World Health Organization; 2022.
Bachelerie F, Ben-Baruch A, Burkhardt AM, Combadiere C, Farber JM, Graham GJ, et al. International Union of Basic and Clinical Pharmacology. [corrected]. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacol Rev. 2014;66:1–79.
Adams JH, Hudson DE, Torii M, Ward GE, Wellems TE, Aikawa M, et al. The Duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell. 1990;63:141–53.
Google Scholar
Adams JH, Sim BK, Dolan SA, Fang X, Kaslow DC, Miller LH. A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci USA. 1992;89:7085–9.
Google Scholar
Wertheimer SP, Barnwell JW. Plasmodium vivax interaction with the human Duffy blood group glycoprotein: identification of a parasite receptor-like protein. Exp Parasitol. 1989;69:340–50.
Google Scholar
Batchelor JD, Malpede BM, Omattage NS, DeKoster GT, Henzler-Wildman KA, Tolia NH. Red blood cell invasion by Plasmodium vivax: structural basis for DBP engagement of DARC. PLoS Pathog. 2014;10: e1003869.
Google Scholar
Batchelor JD, Zahm JA, Tolia NH. Dimerization of Plasmodium vivax DBP is induced upon receptor binding and drives recognition of DARC. Nat Struct Mol Biol. 2011;18:908–14.
Google Scholar
Chitnis CE, Chaudhuri A, Horuk R, Pogo AO, Miller LH. The domain on the Duffy blood group antigen for binding Plasmodium vivax and P. knowlesi malarial parasites to erythrocytes. J Exp Med. 1996;184:1531–6.
Google Scholar
Chitnis CE, Miller LH. Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. J Exp Med. 1994;180:497–506.
Google Scholar
Hans D, Pattnaik P, Bhattacharyya A, Shakri AR, Yazdani SS, Sharma M, et al. Mapping binding residues in the Plasmodium vivax domain that binds Duffy antigen during red cell invasion. Mol Microbiol. 2005;55:1423–34.
Google Scholar
Gosi P, Khusmith S, Khalambaheti T, Lanar DE, Schaecher KE, Fukuda MM, et al. Polymorphism patterns in Duffy-binding protein among Thai Plasmodium vivax isolates. Malar J. 2008;7:112.
Google Scholar
Xainli J, Adams JH, King CL. The erythrocyte binding motif of Plasmodium vivax Duffy binding protein is highly polymorphic and functionally conserved in isolates from Papua New Guinea. Mol Biochem Parasitol. 2000;111:253–60.
Google Scholar
Chootong P, Ntumngia FB, VanBuskirk KM, Xainli J, Cole-Tobian JL, Campbell CO, et al. Mapping epitopes of the Plasmodium vivax Duffy binding protein with naturally acquired inhibitory antibodies. Infect Immun. 2010;78:1089–95.
Google Scholar
Patarroyo MA, Molina-Franky J, Gomez M, Arevalo-Pinzon G, Patarroyo ME. Hotspots in Plasmodium and RBC receptor-ligand interactions: key pieces for inhibiting malarial parasite invasion. Int J Mol Sci. 2020;21:4729.
Google Scholar
Roesch C, Popovici J, Bin S, Run V, Kim S, Ramboarina S, et al. Genetic diversity in two Plasmodium vivax protein ligands for reticulocyte invasion. PLoS Negl Trop Dis. 2018;12: e0006555.
Google Scholar
Hou MM, Barrett JR, Themistocleous Y, Rawlinson TA, Diouf A, Martinez FJ, et al. Impact of a blood-stage vaccine on Plasmodium vivax malaria. MedRxiv. 2022. https://doi.org/10.1101/2022.05.27.22275375.
Google Scholar
Chen E, Salinas ND, Huang Y, Ntumngia F, Plasencia MD, Gross ML, et al. Broadly neutralizing epitopes in the Plasmodium vivax vaccine candidate Duffy Binding Protein. Proc Natl Acad Sci USA. 2016;113:6277–82.
Google Scholar
Ntumngia FB, Schloegel J, Barnes SJ, McHenry AM, Singh S, King CL, et al. Conserved and variant epitopes of Plasmodium vivax Duffy binding protein as targets of inhibitory monoclonal antibodies. Infect Immun. 2012;80:1203–8.
Google Scholar
Urusova D, Carias L, Huang Y, Nicolete VC, Popovici J, Roesch C, et al. Author correction: structural basis for neutralization of Plasmodium vivax by naturally acquired human antibodies that target DBP. Nat Microbiol. 2019;4:2024.
Google Scholar
King CL, Michon P, Shakri AR, Marcotty A, Stanisic D, Zimmerman PA, et al. Naturally acquired Duffy-binding protein-specific binding inhibitory antibodies confer protection from blood-stage Plasmodium vivax infection. Proc Natl Acad Sci USA. 2008;105:8363–8.
Google Scholar
Lin E, Kiniboro B, Gray L, Dobbie S, Robinson L, Laumaea A, et al. Differential patterns of infection and disease with P. falciparum and P. vivax in young Papua New Guinean children. PLoS ONE. 2010;5:e9047.
Google Scholar
Chootong P, Panichakul T, Permmongkol C, Barnes SJ, Udomsangpetch R, Adams JH. Characterization of inhibitory anti-Duffy binding protein II immunity: approach to Plasmodium vivax vaccine development in Thailand. PLoS ONE. 2012;7: e35769.
Google Scholar
de Sousa TN, Kano FS, de Brito CF, Carvalho LH. The Duffy binding protein as a key target for a Plasmodium vivax vaccine: lessons from the Brazilian Amazon. Mem Inst Oswaldo Cruz. 2014;109:608–17.
Google Scholar
Nicolete VC, Frischmann S, Barbosa S, King CL, Ferreira MU. Naturally acquired binding-inhibitory antibodies to Plasmodium vivax Duffy Binding Protein and clinical immunity to malaria in rural Amazonians. J Infect Dis. 2016;214:1539–46.
Google Scholar
Carias LL, Dechavanne S, Nicolete VC, Sreng S, Suon S, Amaratunga C, et al. Identification and characterization of functional human monoclonal antibodies to Plasmodium vivax Duffy-Binding Protein. J Immunol. 2019;202:2648–60.
Google Scholar
Payne RO, Silk SE, Elias SC, Milne KH, Rawlinson TA, Llewellyn D, et al. Human vaccination against Plasmodium vivax Duffy-binding protein induces strain-transcending antibodies. JCI Insight. 2017;2: e93683.
Google Scholar
Gruring C, Moon RW, Lim C, Holder AA, Blackman MJ, Duraisingh MT. Human red blood cell-adapted Plasmodium knowlesi parasites: a new model system for malaria research. Cell Microbiol. 2014;16:612–20.
Google Scholar
Mohring F, Hart MN, Patel A, Baker DA, Moon RW. CRISPR-Cas9 genome editing of Plasmodium knowlesi. Bio Protoc. 2020;10: e3522.
Google Scholar
Moon RW, Hall J, Rangkuti F, Ho YS, Almond N, Mitchell GH, et al. Adaptation of the genetically tractable malaria pathogen Plasmodium knowlesi to continuous culture in human erythrocytes. Proc Natl Acad Sci USA. 2013;110:531–6.
Google Scholar
Rawlinson TA, Barber NM, Mohring F, Cho JS, Kosaisavee V, Gerard SF, et al. Structural basis for inhibition of Plasmodium vivax invasion by a broadly neutralizing vaccine-induced human antibody. Nat Microbiol. 2019;4:1497–507.
Google Scholar
Menard D, Barnadas C, Bouchier C, Henry-Halldin C, Gray LR, Ratsimbasoa A, et al. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci USA. 2010;107:5967–71.
Google Scholar
Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, Wardemann H. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods. 2008;329:112–24.
Google Scholar
Wardemann H, Kofer J. Expression cloning of human B cell immunoglobulins. Methods Mol Biol. 2013;971:93–111.
Google Scholar
Smolarek D, Hattab C, Hassanzadeh-Ghassabeh G, Cochet S, Gutierrez C, de Brevern AG, et al. A recombinant dromedary antibody fragment (VHH or nanobody) directed against human Duffy antigen receptor for chemokines. Cell Mol Life Sci. 2010;67:3371–87.
Google Scholar
Ford TC, Rickwood D. Formation of isotonic Nycodenz gradients for cell separations. Anal Biochem. 1982;124:293–8.
Google Scholar
Popovici J, Roesch C, Carias LL, Khim N, Kim S, Vantaux A, et al. Amplification of Duffy binding protein-encoding gene allows Plasmodium vivax to evade host anti-DBP humoral immunity. Nat Commun. 2020;11:953.
Google Scholar
Rangel GW, Clark MA, Kanjee U, Lim C, Shaw-Saliba K, Menezes MJ, et al. Enhanced ex vivo Plasmodium vivax intraerythrocytic enrichment and maturation for rapid and sensitive parasite growth assays. Antimicrob Agents Chemother. 2018. https://doi.org/10.1128/AAC.02519-17.
Google Scholar
Ianevski A, Giri AK, Aittokallio T. SynergyFinder 2.0: visual analytics of multi-drug combination synergies. Nucleic Acids Res. 2020;48(W1):W488–93.
Google Scholar
Mendoza P, Gruell H, Nogueira L, Pai JA, Butler AL, Millard K, et al. Combination therapy with anti-HIV-1 antibodies maintains viral suppression. Nature. 2018;561:479–84.
Google Scholar
Mulangu S, Dodd LE, Davey RT, Tshiani Mbaya O, Proschan M, Mukadi D, et al. A randomized, controlled trial of Ebola virus disease therapeutics. N Engl J Med. 2019;381:2293–303.
Google Scholar
Weinreich DM, Sivapalasingam S, Norton T, Ali S, Gao H, Bhore R, et al. REGN-COV2, a neutralizing antibody cocktail, in outpatients with Covid-19. N Engl J Med. 2021;384:238–51.
Google Scholar
Singh K, Mukherjee P, Shakri AR, Singh A, Pandey G, Bakshi M, et al. Malaria vaccine candidate based on Duffy-binding protein elicits strain transcending functional antibodies in a Phase I trial. NPJ Vaccines. 2018;3:48.
Google Scholar
Hou MM, Barrett JR, Themistocleous Y, Rawlinson TA, Diouf A, Martinez FJ, et al. Vaccination with Plasmodium vivax Duffy-binding protein inhibits parasite growth during controlled human malaria infection. Sci Transl Med. 2023;15:eadf1782.
Google Scholar
Wang LT, Pereira LS, Flores-Garcia Y, O’Connor J, Flynn BJ, Schön A, et al. A potent anti-malarial human monoclonal antibody targets circumsporozoite protein minor repeats and neutralizes sporozoites in the liver. Immunity. 2020;53:733-44.e8.
Google Scholar
Kisalu NK, Idris AH, Weidle C, Flores-Garcia Y, Flynn BJ, Sack BK, et al. A human monoclonal antibody prevents malaria infection by targeting a new site of vulnerability on the parasite. Nat Med. 2018;24:408–16.
Google Scholar
Kayentao K, Ongoiba A, Preston AC, Healy SA, Doumbo S, Doumtabe D, et al. Safety and efficacy of a monoclonal antibody against malaria in Mali. N Engl J Med. 2022;387:1833–42.
Google Scholar
Gaudinski MR, Berkowitz NM, Idris AH, Coates EE, Holman LA, Mendoza F, et al. A monoclonal antibody for malaria prevention. N Engl J Med. 2021;385:803–14.
Google Scholar
Agudelo M, Muecksch F, Schaefer-Babajew D, Cho A, DaSilva J, Bednarski E, et al. Plasma and memory antibody responses to Gamma SARS-CoV-2 provide limited cross-protection to other variants. J Exp Med. 2022. https://doi.org/10.1084/jem.20220367.
Google Scholar
Ketas TJ, Holuigue S, Matthews K, Moore JP, Klasse PJ. Env-glycoprotein heterogeneity as a source of apparent synergy and enhanced cooperativity in inhibition of HIV-1 infection by neutralizing antibodies and entry inhibitors. Virology. 2012;422:22–36.
Google Scholar
Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, Majeed S, et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature. 2002;420:678–82.
Google Scholar
Ramirez Valdez KP, Kuwata T, Maruta Y, Tanaka K, Alam M, Yoshimura K, et al. Complementary and synergistic activities of anti-V3, CD4bs and CD4i antibodies derived from a single individual can cover a wide range of HIV-1 strains. Virology. 2015;475:187–203.
Google Scholar
Van Rompay KKA, Olstad KJ, Sammak RL, Dutra J, Watanabe JK, Usachenko JL, et al. Early treatment with a combination of two potent neutralizing antibodies improves clinical outcomes and reduces virus replication and lung inflammation in SARS-CoV-2 infected macaques. PLoS Pathog. 2021;17: e1009688.
Google Scholar
Wang LT, Pereira LS, Kiyuka PK, Schon A, Kisalu NK, Vistein R, et al. Protective effects of combining monoclonal antibodies and vaccines against the Plasmodium falciparum circumsporozoite protein. PLoS Pathog. 2021;17: e1010133.
Google Scholar
Willcox AC, Huber AS, Diouf A, Barrett JR, Silk SE, Pulido D, et al. Antibodies from malaria-exposed Malians generally interact additively or synergistically with human vaccine-induced RH5 antibodies. Cell Rep Med. 2021;2: 100326.
Google Scholar
