Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein
Abstract
Acquired resistance against antimalarial drugs has further increased the need for an effective malaria vaccine. The current leading candidate, RTS,S, is a recombinant circumsporozoite protein (CSP)-based vaccine against Plasmodium falciparum that contains 19 NANP repeats followed by a thrombospondin repeat domain. Although RTS,S has undergone extensive clinical testing and has progressed through phase III clinical trials, continued efforts are underway to enhance its efficacy and duration of protection. Here in this paper, we determined that two monoclonal antibodies (mAbs 311 and 317), isolated from a recent controlled human malaria infection trial exploring a delayed fractional dose, inhibit parasite development in vivo by at least 97%. Crystal structures of antibody fragments (Fabs) 311 and 317 with an (NPNA)3 peptide illustrate their different binding modes. Notwithstanding, one and three of the three NPNA repeats adopt similar well-defined type I β-turns with Fab311 and Fab317, respectively. Furthermore, to explore antibody binding in the context of P. falciparum CSP, we used negative-stain electron microscopy on a recombinant shortened CSP (rsCSP) construct saturated with Fabs. Both complexes display a compact rsCSP with multiple Fabs bound, with the rsCSP–Fab311 complex forming a highly organized helical structure. Lastly, together, these structural insights may aid in the designmore »
- Authors:
-
- Scripps Research Inst., La Jolla, CA (United States). Dept. of Integrative Structural and Computational Biology
- PATH Center for Vaccine Innovation and Access, Washington, DC (United States). PATH's Malaria Vaccine Initiative
- Atreca Inc., Redwood City, CA (United States)
- Stanford Univ., CA (United States). Dept. of Microbiology and Immunology
- Johns Hopkins Univ., Baltimore, MD (United States). Bloomberg School of Public Health, Malaria Research Inst.
- Scripps Research Inst., La Jolla, CA (United States). Dept. of Integrative Structural and Computational Biology; Scripps Research Inst., La Jolla, CA (United States). Skaggs Inst. for Chemical Biology
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
- OSTI Identifier:
- 1423464
- Grant/Contract Number:
- AC02-76SF00515; AI44375; P41GM103393; AC02-06CH11357; 1S10OD012289-01A1
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 114; Journal Issue: 48; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences, Washington, DC (United States)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; malaria; circumsporozoite protein; antibodies; X-ray crystallography; EM
Citation Formats
Oyen, David, Torres, Jonathan L., Wille-Reece, Ulrike, Ockenhouse, Christian F., Emerling, Daniel, Glanville, Jacob, Volkmuth, Wayne, Flores-Garcia, Yevel, Zavala, Fidel, Ward, Andrew B., King, C. Richter, and Wilson, Ian A. Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein. United States: N. p., 2017.
Web. doi:10.1073/pnas.1715812114.
Oyen, David, Torres, Jonathan L., Wille-Reece, Ulrike, Ockenhouse, Christian F., Emerling, Daniel, Glanville, Jacob, Volkmuth, Wayne, Flores-Garcia, Yevel, Zavala, Fidel, Ward, Andrew B., King, C. Richter, & Wilson, Ian A. Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein. United States. https://doi.org/10.1073/pnas.1715812114
Oyen, David, Torres, Jonathan L., Wille-Reece, Ulrike, Ockenhouse, Christian F., Emerling, Daniel, Glanville, Jacob, Volkmuth, Wayne, Flores-Garcia, Yevel, Zavala, Fidel, Ward, Andrew B., King, C. Richter, and Wilson, Ian A. Tue .
"Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein". United States. https://doi.org/10.1073/pnas.1715812114. https://www.osti.gov/servlets/purl/1423464.
@article{osti_1423464,
title = {Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein},
author = {Oyen, David and Torres, Jonathan L. and Wille-Reece, Ulrike and Ockenhouse, Christian F. and Emerling, Daniel and Glanville, Jacob and Volkmuth, Wayne and Flores-Garcia, Yevel and Zavala, Fidel and Ward, Andrew B. and King, C. Richter and Wilson, Ian A.},
abstractNote = {Acquired resistance against antimalarial drugs has further increased the need for an effective malaria vaccine. The current leading candidate, RTS,S, is a recombinant circumsporozoite protein (CSP)-based vaccine against Plasmodium falciparum that contains 19 NANP repeats followed by a thrombospondin repeat domain. Although RTS,S has undergone extensive clinical testing and has progressed through phase III clinical trials, continued efforts are underway to enhance its efficacy and duration of protection. Here in this paper, we determined that two monoclonal antibodies (mAbs 311 and 317), isolated from a recent controlled human malaria infection trial exploring a delayed fractional dose, inhibit parasite development in vivo by at least 97%. Crystal structures of antibody fragments (Fabs) 311 and 317 with an (NPNA)3 peptide illustrate their different binding modes. Notwithstanding, one and three of the three NPNA repeats adopt similar well-defined type I β-turns with Fab311 and Fab317, respectively. Furthermore, to explore antibody binding in the context of P. falciparum CSP, we used negative-stain electron microscopy on a recombinant shortened CSP (rsCSP) construct saturated with Fabs. Both complexes display a compact rsCSP with multiple Fabs bound, with the rsCSP–Fab311 complex forming a highly organized helical structure. Lastly, together, these structural insights may aid in the design of a next-generation malaria vaccine.},
doi = {10.1073/pnas.1715812114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 48,
volume = 114,
place = {United States},
year = {Tue Nov 14 00:00:00 EST 2017},
month = {Tue Nov 14 00:00:00 EST 2017}
}
Web of Science
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- van der Kant, Rob; Bauer, Joschka; Karow-Zwick, Anne R.
- Protein Engineering, Design and Selection, Vol. 32, Issue 3
Antihomotypic affinity maturation improves human B cell responses against a repetitive epitope
journal, June 2018
- Imkeller, Katharina; Scally, Stephen W.; Bosch, Alexandre
- Science, Vol. 360, Issue 6395
Chimeric Plasmodium falciparum parasites expressing Plasmodium vivax circumsporozoite protein fail to produce salivary gland sporozoites
journal, August 2018
- Marin-Mogollon, Catherin; van Pul, Fiona J. A.; Miyazaki, Shinya
- Malaria Journal, Vol. 17, Issue 1
Optimization of an in vivo model to study immunity to Plasmodium falciparum pre-erythrocytic stages
journal, December 2019
- Flores-Garcia, Yevel; Herrera, Sonia M.; Jhun, Hugo
- Malaria Journal, Vol. 18, Issue 1
Plasmodium falciparum pre-erythrocytic stage vaccine development
journal, February 2020
- Molina-Franky, Jessica; Cuy-Chaparro, Laura; Camargo, Anny
- Malaria Journal, Vol. 19, Issue 1
Reassessing therapeutic antibodies for neglected and tropical diseases
journal, January 2020
- Hooft van Huijsduijnen, Rob; Kojima, Somei; Carter, Dee
- PLOS Neglected Tropical Diseases, Vol. 14, Issue 1
Structure and mechanism of monoclonal antibody binding to the junctional epitope of Plasmodium falciparum circumsporozoite protein
journal, March 2020
- Oyen, David; Torres, Jonathan L.; Aoto, Phillip C.
- PLOS Pathogens, Vol. 16, Issue 3