Development of an improved blood-stage malaria vaccine targeting the essential RH5-CyRPA-RIPR invasion complex

Author:

Williams Barnabas G.ORCID,King Lloyd D. W.,Pulido David,Quinkert Doris,Lias Amelia M.,Silk Sarah E.,Ragotte Robert J.,Davies Hannah,Barrett Jordan R.,McHugh KirstyORCID,Rigby Cassandra A.,Alanine Daniel G. W.,Barfod Lea,Shea Michael W.,Cowley Li An,Dabbs Rebecca A.,Pattinson David J.,Douglas Alexander D.,Lyth Oliver R.,Illingworth Joseph J.,Jin Jing,Carnrot Cecilia,Kotraiah Vinayaka,Christen Jayne M.,Noe Amy R.,MacGill Randall S.,King C. Richter,Birkett Ashley J.,Soisson Lorraine A.,Skinner Katherine,Miura Kazutoyo,Long Carole A.,Higgins Matthew K.ORCID,Draper Simon J.ORCID

Abstract

ABSTRACTIn recent years, reticulocyte-binding protein homologue 5 (RH5) has emerged as a leading blood-stagePlasmodium falciparummalaria vaccine antigen. The most advanced blood-stage vaccine candidate in a Phase 2b clinical trial, RH5.1/Matrix-M™, is based on a full-length soluble protein-with-adjuvant formulation. RH5 interacts with cysteine-rich protective antigen (CyRPA) and RH5- interacting protein (RIPR) to form an essential heterotrimeric “RCR-complex”. Here, we investigated whether a vaccine candidate based on the ternary RCR-complex could substantially improve upon the leading clinical candidate RH5.1/Matrix-M™ in preclinical studies. Using a panel of monoclonal antibodies (mAbs) we confirm that parasite growth-inhibitory epitopes on each antigen are exposed on the surface of the RCR-complex and that mAb pairs binding to different antigens can function additively or synergistically to mediate parasite growth inhibition activity (GIA)in vitro. However, immunisation of rats with the RCR-complex consistently fails to outperform RH5.1 alone. We show this is due to immuno-dominance of RIPR coupled with the inferior potency of anti-full length RIPR polyclonal IgG antibodies as compared to the anti-RH5 and anti-CyRPA response. To address this, we identified the growth-inhibitory antibody epitopes of RIPR are clustered within C-terminal EGF-like domains of RIPR. A fusion of these EGF domains to CyRPA, called “R78C”, combined with RH5.1, provided a new vaccination strategy that improves upon the levels ofin vitroGIA seen with RH5.1 alone. Superiority of the combination antigen vaccine candidate was achieved by the induction of a quantitatively higher, but qualitatively similar, polyclonal antibody response that demonstrated additive GIA across the three antigen targets. These preclinical data justified the advancement of the RH5.1+R78C/Matrix-M™ combination vaccine to a Phase 1 clinical trial.

Publisher

Cold Spring Harbor Laboratory

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