A novel CSP C-terminal epitope targeted by an antibody with protective activity against Plasmodium falciparum

Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf). RTS,S/AS01 is the first, and to date, the only vaccine that has demonstrated significant reduction of clinical and severe malaria in endemic cohorts in Phase 3 trials. Although the vacc...

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Published inPLoS pathogens Vol. 18; no. 3; p. e1010409
Main Authors Beutler, Nathan, Pholcharee, Tossapol, Oyen, David, Flores-Garcia, Yevel, MacGill, Randall S, Garcia, Elijah, Calla, Jaeson, Parren, Mara, Yang, Linlin, Volkmuth, Wayne, Locke, Emily, Regules, Jason A, Dutta, Sheetij, Emerling, Daniel, Early, Angela M, Neafsey, Daniel E, Winzeler, Elizabeth A, King, C Richter, Zavala, Fidel, Burton, Dennis R, Wilson, Ian A, Rogers, Thomas F
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.03.2022
Public Library of Science (PLoS)
Subjects
Animal models
Animals
Antibodies
Antibodies, Protozoan
Antigenic determinants
Biology and Life Sciences
Circumsporozoite protein
Clinical trials
Competition
Crystal structure
Drug dosages
Epitopes
Experiments
Gene expression
Genetic aspects
Health aspects
Heparan sulfate
Humans
Immune response
Immunization
Interferometry
Malaria
Malaria Vaccines
Malaria, Falciparum - prevention & control
Medicine and Health Sciences
Mice
Monoclonal antibodies
Peptides
Physical Sciences
Plasmodium falciparum
Protozoan Proteins - genetics
Sensors
Vaccines
Vector-borne diseases
United States
Africa
Online AccessGet full text

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Abstract Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf). RTS,S/AS01 is the first, and to date, the only vaccine that has demonstrated significant reduction of clinical and severe malaria in endemic cohorts in Phase 3 trials. Although the vaccine is protective, efficacy declines over time with kinetics paralleling the decline in antibody responses to the Pf circumsporozoite protein (PfCSP). Although most attention has focused on antibodies to repeat motifs on PfCSP, antibodies to other regions may play a role in protection. Here, we expressed and characterized seven monoclonal antibodies to the C-terminal domain of CSP (ctCSP) from volunteers immunized with RTS,S/AS01. Competition and crystal structure studies indicated that the antibodies target two different sites on opposite faces of ctCSP. One site contains a polymorphic region (denoted α-ctCSP) and has been previously characterized, whereas the second is a previously undescribed site on the conserved β-sheet face of the ctCSP (denoted β-ctCSP). Antibodies to the β-ctCSP site exhibited broad reactivity with a diverse panel of ctCSP peptides whose sequences were derived from field isolates of P. falciparum whereas antibodies to the α-ctCSP site showed very limited cross reactivity. Importantly, an antibody to the β-site demonstrated inhibition activity against malaria infection in a murine model. This study identifies a previously unidentified conserved epitope on CSP that could be targeted by prophylactic antibodies and exploited in structure-based vaccine design.
AbstractList Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf). RTS,S/AS01 is the first, and to date, the only vaccine that has demonstrated significant reduction of clinical and severe malaria in endemic cohorts in Phase 3 trials. Although the vaccine is protective, efficacy declines over time with kinetics paralleling the decline in antibody responses to the Pf circumsporozoite protein (PfCSP). Although most attention has focused on antibodies to repeat motifs on PfCSP, antibodies to other regions may play a role in protection. Here, we expressed and characterized seven monoclonal antibodies to the C-terminal domain of CSP (ctCSP) from volunteers immunized with RTS,S/AS01. Competition and crystal structure studies indicated that the antibodies target two different sites on opposite faces of ctCSP. One site contains a polymorphic region (denoted α-ctCSP) and has been previously characterized, whereas the second is a previously undescribed site on the conserved β-sheet face of the ctCSP (denoted β-ctCSP). Antibodies to the β-ctCSP site exhibited broad reactivity with a diverse panel of ctCSP peptides whose sequences were derived from field isolates of P. falciparum whereas antibodies to the α-ctCSP site showed very limited cross reactivity. Importantly, an antibody to the β-site demonstrated inhibition activity against malaria infection in a murine model. This study identifies a previously unidentified conserved epitope on CSP that could be targeted by prophylactic antibodies and exploited in structure-based vaccine design.
Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf) . RTS,S/AS01 is the first, and to date, the only vaccine that has demonstrated significant reduction of clinical and severe malaria in endemic cohorts in Phase 3 trials. Although the vaccine is protective, efficacy declines over time with kinetics paralleling the decline in antibody responses to the Pf circumsporozoite protein ( Pf CSP). Although most attention has focused on antibodies to repeat motifs on Pf CSP, antibodies to other regions may play a role in protection. Here, we expressed and characterized seven monoclonal antibodies to the C-terminal domain of CSP (ctCSP) from volunteers immunized with RTS,S/AS01. Competition and crystal structure studies indicated that the antibodies target two different sites on opposite faces of ctCSP. One site contains a polymorphic region (denoted α-ctCSP) and has been previously characterized, whereas the second is a previously undescribed site on the conserved β-sheet face of the ctCSP (denoted β-ctCSP). Antibodies to the β-ctCSP site exhibited broad reactivity with a diverse panel of ctCSP peptides whose sequences were derived from field isolates of P . falciparum whereas antibodies to the α-ctCSP site showed very limited cross reactivity. Importantly, an antibody to the β-site demonstrated inhibition activity against malaria infection in a murine model. This study identifies a previously unidentified conserved epitope on CSP that could be targeted by prophylactic antibodies and exploited in structure-based vaccine design. The most advanced malaria vaccine candidate to date, RTS,S, is composed of the central repeat region, so called because it consists of repeats of an NANP amino-acid sequence, and the C-terminal domain from the Plasmodium falciparum circumsporozoite protein ( Pf CSP). RTS,S is about 50% effective against the liver stage of the malaria parasite, but its efficacy decreases over time, concomitant with waning of antibodies that target Pf CSP. Thus, further understanding of which antibodies are effective in the immune response to Pf CSP is needed to facilitate design of next-generation malaria vaccines. While much is known about antibodies to the NANP repeat region, the nature and efficacy of antibodies that target the Pf CSP C-terminal domain (ctCSP) is underexplored. Here, we characterize antibodies against ctCSP that were derived from volunteers in a phase 2a trial of RTS,S with a fractional dose regimen. We find that some antibodies bind to a previously identified polymorphic site on ctCSP, but others bind to a novel site that is highly conserved across different P . falciparum isolates. Furthermore, these antibodies show protection against P . falciparum infection in a mouse model. Thus, a previously unidentified and conserved site on ctCSP can be targeted by antibodies and will aid in design of more effective next-generation Pf CSP-based malaria vaccines and therapeutics.
Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf) . RTS,S/AS01 is the first, and to date, the only vaccine that has demonstrated significant reduction of clinical and severe malaria in endemic cohorts in Phase 3 trials. Although the vaccine is protective, efficacy declines over time with kinetics paralleling the decline in antibody responses to the Pf circumsporozoite protein ( Pf CSP). Although most attention has focused on antibodies to repeat motifs on Pf CSP, antibodies to other regions may play a role in protection. Here, we expressed and characterized seven monoclonal antibodies to the C-terminal domain of CSP (ctCSP) from volunteers immunized with RTS,S/AS01. Competition and crystal structure studies indicated that the antibodies target two different sites on opposite faces of ctCSP. One site contains a polymorphic region (denoted α-ctCSP) and has been previously characterized, whereas the second is a previously undescribed site on the conserved β-sheet face of the ctCSP (denoted β-ctCSP). Antibodies to the β-ctCSP site exhibited broad reactivity with a diverse panel of ctCSP peptides whose sequences were derived from field isolates of P . falciparum whereas antibodies to the α-ctCSP site showed very limited cross reactivity. Importantly, an antibody to the β-site demonstrated inhibition activity against malaria infection in a murine model. This study identifies a previously unidentified conserved epitope on CSP that could be targeted by prophylactic antibodies and exploited in structure-based vaccine design.
Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf). RTS,S/AS01 is the first, and to date, the only vaccine that has demonstrated significant reduction of clinical and severe malaria in endemic cohorts in Phase 3 trials. Although the vaccine is protective, efficacy declines over time with kinetics paralleling the decline in antibody responses to the Pf circumsporozoite surface protein (PfCSP). Although most attention has focused on antibodies to repeat motifs on PfCSP, antibodies to other regions may play a role in protection. Here, we expressed and characterized seven monoclonal antibodies to the C-terminal domain of CSP (ctCSP) from volunteers immunized with RTS,S/AS01. Competition and crystal structure studies indicated that the antibodies target two different sites on opposite faces of ctCSP. One site contains a polymorphic region (denoted [alpha]-ctCSP) and has been previously characterized, whereas the second is a previously undescribed site on the conserved [beta]-sheet face of the ctCSP (denoted [beta]-ctCSP). Antibodies to the [beta]-ctCSP site exhibited broad reactivity with a diverse panel of ctCSP peptides whose sequences were derived from field isolates of P. falciparum whereas antibodies to the [alpha]-ctCSP site showed very limited cross reactivity. Importantly, an antibody to the [beta]-site demonstrated inhibition activity against malaria infection in a murine model. This study identifies a previously unidentified conserved epitope on CSP that could be targeted by prophylactic antibodies and exploited in structure-based vaccine design.
Audience Academic
Author Wilson, Ian A
Neafsey, Daniel E
Emerling, Daniel
Volkmuth, Wayne
Flores-Garcia, Yevel
Oyen, David
Winzeler, Elizabeth A
Zavala, Fidel
Parren, Mara
Locke, Emily
Rogers, Thomas F
MacGill, Randall S
Pholcharee, Tossapol
Dutta, Sheetij
Early, Angela M
Garcia, Elijah
Regules, Jason A
Beutler, Nathan
Calla, Jaeson
King, C Richter
Yang, Linlin
Burton, Dennis R
AuthorAffiliation 6 Atreca Inc., South San Francisco, California, United States of America
8 Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, United States of America
7 Malaria Biologics Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America
10 Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology, and Harvard University, Cambridge, Massachusetts, United States of America
11 The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, California, United States of America
2 Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, California, United States of America
3 Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America
The Walter and Eliza Hall Institute of Medical Research, AUSTRALIA
9 Department of Immunology and Infectious Diseases, Har
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Current address: Bluestar Genomics, San Mateo, California, United States of America.
Current address: Pfizer Inc., San Diego, California, United States of America.
We have read the journal’s policy and the authors of this manuscript have the following competing interests. The authors N.B., T.P., D.O., Y.F.G., R.S.M., E.G., J.C., M.P., L.Y., E.L., J.A.R., S.D., A.M.E., D.E.N., E.W., C.R.K., F.Z., D.R.B., I.A.W., and T.F.R. declare that they have no competing interests. W.V., D.E. were or are employees of Atreca, Inc. and own equity in Atreca, Inc.
Current address: Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
ORCID 0000-0002-6469-2419
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Snippet Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf). RTS,S/AS01 is the first, and to date, the...
Potent and durable vaccine responses will be required for control of malaria caused by Plasmodium falciparum (Pf) . RTS,S/AS01 is the first, and to date, the...
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StartPage e1010409
SubjectTerms Animal models
Animals
Antibodies
Antibodies, Protozoan
Antigenic determinants
Biology and Life Sciences
Circumsporozoite protein
Clinical trials
Competition
Crystal structure
Drug dosages
Epitopes
Experiments
Gene expression
Genetic aspects
Health aspects
Heparan sulfate
Humans
Immune response
Immunization
Interferometry
Malaria
Malaria Vaccines
Malaria, Falciparum - prevention & control
Medicine and Health Sciences
Mice
Monoclonal antibodies
Peptides
Physical Sciences
Plasmodium falciparum
Protozoan Proteins - genetics
Sensors
Vaccines
Vector-borne diseases
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Title A novel CSP C-terminal epitope targeted by an antibody with protective activity against Plasmodium falciparum
URI https://www.ncbi.nlm.nih.gov/pubmed/35344575
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http://dx.doi.org/10.1371/journal.ppat.1010409
Volume 18
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