Authors

Valentina Ceglia, Baylor Scott and White Research Institute, Dallas, TX, United States; Université Paris-Est Créteil, Sciences de la Vie et de la Santé, Créteil, France; Vaccine Research Institute, The Institut National de la Santé et de la Recherche Médicale (INSERM), Unité U955, Institut Mondor de Recherche Biomédicale, Créteil, France
Sandra Zurawski, Baylor Scott and White Research Institute, Dallas, TX, United States; Vaccine Research Institute, The Institut National de la Santé et de la Recherche Médicale (INSERM), Unité U955, Institut Mondor de Recherche Biomédicale, Créteil, France
Monica Montes, Baylor Scott and White Research Institute, Dallas, TX, United States; Vaccine Research Institute, The Institut National de la Santé et de la Recherche Médicale (INSERM), Unité U955, Institut Mondor de Recherche Biomédicale, Créteil, France
Mitchell Kroll, Baylor Scott and White Research Institute, Dallas, TX, United States; Institute of Biomedical Studies, Baylor University, Waco, TX, United States
Aurélie Bouteau, Institute of Biomedical Studies, Baylor University, Waco, TX, United States; Department of Microbiology and Immunology, Thomas Jefferson University, Philadelphia, PA, United States
Zhiqing Wang, Baylor Scott and White Research Institute, Dallas, TX, United States; Vaccine Research Institute, The Institut National de la Santé et de la Recherche Médicale (INSERM), Unité U955, Institut Mondor de Recherche Biomédicale, Créteil, France
Jerome Ellis, Baylor Scott and White Research Institute, Dallas, TX, United States; Vaccine Research Institute, The Institut National de la Santé et de la Recherche Médicale (INSERM), Unité U955, Institut Mondor de Recherche Biomédicale, Créteil, France
Botond Z Igyártó, Baylor Scott and White Research Institute, Dallas, TX, United States; Department of Microbiology and Immunology, Thomas Jefferson University, Philadelphia, PA, United States
Yves Lévy, Université Paris-Est Créteil, Sciences de la Vie et de la Santé, Créteil, France; Vaccine Research Institute, The Institut National de la Santé et de la Recherche Médicale (INSERM), Unité U955, Institut Mondor de Recherche Biomédicale, Créteil, France
Gerard Zurawski, Baylor Scott and White Research Institute, Dallas, TX, United States; Vaccine Research Institute, The Institut National de la Santé et de la Recherche Médicale (INSERM), Unité U955, Institut Mondor de Recherche Biomédicale, Créteil, France

Document Type

Article

Publication Date

1-13-2022

Comments

This article is the author's final published version in Frontiers in Immunology, Volume 12, January 2022, Article number 786144.

The published version is available at https://doi.org/10.3389/fimmu.2021.786144.

© 2022 Ceglia, Zurawski, Montes, Kroll, Bouteau, Wang, Ellis, Igyártó, Lévy and Zurawski This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Abstract

CD40 is a potent activating receptor expressed on antigen-presenting cells (APCs) of the immune system. CD40 regulates many aspects of B and T cell immunity via interaction with CD40L expressed on activated T cells. Targeting antigens to CD40 via agonistic anti-CD40 antibody fusions promotes both humoral and cellular immunity, but current anti-CD40 antibody-antigen vaccine prototypes require co-adjuvant administration for significant in vivo efficacy. This may be a consequence of dulling of anti-CD40 agonist activity via antigen fusion. We previously demonstrated that direct fusion of CD40L to anti-CD40 antibodies confers superagonist properties. Here we show that anti-CD40-CD40L-antigen fusion constructs retain strong agonist activity, particularly for activation of dendritic cells (DCs). Therefore, we tested anti-CD40-CD40L antibody fused to antigens for eliciting immune responses in vitro and in vivo. In PBMC cultures from HIV-1-infected donors, anti-CD40-CD40L fused to HIV-1 antigens preferentially expanded HIV-1-specific CD8+ T cells versus CD4+ T cells compared to analogous anti-CD40-antigen constructs. In normal donors, anti-CD40-CD40L-mediated delivery of Influenza M1 protein elicited M1-specific T cell expansion at lower doses compared to anti-CD40-mediated delivery. Also, on human myeloid-derived dendritic cells, anti-CD40-CD40L-melanoma gp100 peptide induced more sustained Class I antigen presentation compared to anti-CD40-gp100 peptide. In human CD40 transgenic mice, anti-CD40-CD40L-HIV-1 gp140 administered without adjuvant elicited superior antibody responses compared to anti-CD40-gp140 antigen without fused CD40L. In human CD40 mice, compared to the anti-CD40 vehicle, anti-CD40-CD40L delivery of Eα 52-68 peptide elicited proliferating of TCR I-Eα 52-68 CD4+ T cells producing cytokine IFNγ. Also, compared to controls, only anti-CD40-CD40L-Cyclin D1 vaccination of human CD40 mice reduced implanted EO771.LMB breast tumor cell growth. These data demonstrate that human CD40-CD40L antibody fused to antigens maintains highly agonistic activity and generates immune responses distinct from existing low agonist anti-CD40 targeting formats. These advantages were in vitro skewing responses towards CD8+ T cells, increased efficacy at low doses, and longevity of MHC Class I peptide display; and in mouse models, a more robust humoral response, more activated CD4+ T cells, and control of tumor growth. Thus, the anti-CD40-CD40L format offers an alternate DC-targeting platform with unique properties, including intrinsic adjuvant activity.

Creative Commons License

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.

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PubMed ID

35095862

Language

English

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