TY - JOUR
T1 - Combinatorial Resurfacing of Dengue Envelope Protein Domain III Antigens Selectively Ablates Epitopes Associated with Serotype-Specific or Infection-Enhancing Antibody Responses
AU - Remmel, Jennifer L.
AU - Beauchemin, Kathryn S.
AU - Mishra, Akaash K.
AU - Frei, Julia C.
AU - Lai, Jonathan R.
AU - Bailey-Kellogg, Chris
AU - Ackerman, Margaret E.
N1 - Funding Information:
J.L.R. acknowledges support from the National Institutes of Health National Institute of Allergy and Infectious Disease [1F31AI45106]. J.L.R., M.E.A., and C.B.-K. acknowledge support from the National Institute of General Medical Sciences [P20GM113132]. J.R.L. acknowledges support from the National Institutes of Health National Institute of Allergy and Infectious Disease [R21-AI128090]. J.C.F. acknowledges support from the National Institutes of Health National Institute of General Medical Sciences [T32-GM007491].
Publisher Copyright:
Copyright © 2020 American Chemical Society.
PY - 2020/9/14
Y1 - 2020/9/14
N2 - Mutagenesis of surface-exposed residues, or "resurfacing", is a protein engineering strategy that can be utilized to disrupt antibody recognition or modulate the capacity of a protein to elicit antibody responses. We apply resurfacing to engineer Dengue virus envelope protein domain III (DENV DIII) antigens with the goal of focusing humoral recognition on epitopes of interest by selective ablation of irrelevant and undesired epitopes. Cross-reactive but non-neutralizing antibodies have the potential to enhance Dengue virus (DENV) infection by a process called antibody-dependent enhancement, thought to be associated with severe secondary heterotypic infection. Thus, a focus on epitopes associated with broadly neutralizing antibodies is important both for understanding human antibody responses against DENV and for the development of a successful DENV vaccine. To engineer DENV DIII antigens focusing on the AG strand epitope associated with broadly neutralizing antibody responses, we generated yeast surface display libraries of DENV2 DIII where the AB loop (associated with cross-reactive but non-neutralizing antibody responses) and FG loop (associated with serotype-specific antibody responses) were mutagenized to allow for all possible amino acid substitutions. Loop variants that maintained the AG strand epitope and simultaneously disrupted the AB and FG loop epitopes exhibited high and diverse mutational loads that were amenable to loop exchange and transplantation into a DENV4 DIII background. Thus, several loop variants fulfill this antigenicity criteria regardless of serotype context. The resulting resurfaced DIII antigens may be utilized as AG strand epitope-focusing probes or immunogen candidates.
AB - Mutagenesis of surface-exposed residues, or "resurfacing", is a protein engineering strategy that can be utilized to disrupt antibody recognition or modulate the capacity of a protein to elicit antibody responses. We apply resurfacing to engineer Dengue virus envelope protein domain III (DENV DIII) antigens with the goal of focusing humoral recognition on epitopes of interest by selective ablation of irrelevant and undesired epitopes. Cross-reactive but non-neutralizing antibodies have the potential to enhance Dengue virus (DENV) infection by a process called antibody-dependent enhancement, thought to be associated with severe secondary heterotypic infection. Thus, a focus on epitopes associated with broadly neutralizing antibodies is important both for understanding human antibody responses against DENV and for the development of a successful DENV vaccine. To engineer DENV DIII antigens focusing on the AG strand epitope associated with broadly neutralizing antibody responses, we generated yeast surface display libraries of DENV2 DIII where the AB loop (associated with cross-reactive but non-neutralizing antibody responses) and FG loop (associated with serotype-specific antibody responses) were mutagenized to allow for all possible amino acid substitutions. Loop variants that maintained the AG strand epitope and simultaneously disrupted the AB and FG loop epitopes exhibited high and diverse mutational loads that were amenable to loop exchange and transplantation into a DENV4 DIII background. Thus, several loop variants fulfill this antigenicity criteria regardless of serotype context. The resulting resurfaced DIII antigens may be utilized as AG strand epitope-focusing probes or immunogen candidates.
KW - directed evolution
KW - epitope-focusing
KW - immunogen design
KW - protein resurfacing
KW - saturation mutagenesis
KW - yeast surface display
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U2 - 10.1021/acscombsci.0c00073
DO - 10.1021/acscombsci.0c00073
M3 - Article
C2 - 32574486
AN - SCOPUS:85090882404
SN - 2156-8952
VL - 22
SP - 446
EP - 456
JO - Journal of Combinatorial Chemistry
JF - Journal of Combinatorial Chemistry
IS - 9
ER -