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An epicutaneous therapeutic pollen-allergen extract delivery system in an allergic rhinitis mouse model: based on allergen loading on DC-specific aptamers conjugated nanogolds

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Abstract

Background

Gold nanoparticles (GNPs) have previously been suggested as appropriate carriers for allergen-specific immunotherapy (AIT). In this study, we assessed efficacy of GNPs and dendritic cells (DC)-specific aptamer-modified GNPs (Apts-GNP) for epicutaneous immunotherapy (EPIT) in the case of pollen allergen extracts containing a variety of allergenic and non-allergenic components.

Methods

BALB/c mice were sensitized to the total protein extract of Platanus orientalis pollen and epicutaneously treated in different groups either with free P. orientalis total pollen extract, naked GNPs, total extract loaded GNPs, and total extract loaded Apts-GNPs with and without skin-penetrating peptides (SPPs). Then, the specific IgE level (sIgE), total IgE concentration (tIgE) in the serum sample, IL-4, IL-17a, IFN-γ, and IL-10 cytokine concentrations in re-stimulated splenocytes with the total extract and mixture of recombinant allergens, nasopharyngeal lavage fluid (NALF) analysis, and histopathological analysis of lung tissue were evaluated.

Results

This study indicated the total extract-loaded GNPs, especially Pla. ext (50 μg)-GNPs, significantly decreased sIgE, tIgE, IL-17a, and IL-4 concentrations, immune cells and eosinophils infiltration in NALF, and increased IL-10 and IFN-γ concentrations compared with the PBS-treated group. In addition, the histopathological analysis of lung tissue showed a significant decrease in allergic inflammation and histopathological damage. The DC-targeted group revealed the most significant improvement in allergic-related immune factors with no histopathological damage compared with the same dose without aptamer.

Conclusion

Loading total protein extract on the GNPs and the Apt-modified GNPs could be an effective approach to improve EPIT efficacy in a pollen-induced allergic mouse model.

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Acknowledgements

The authors thank Dr. Shaterzade for evaluating lung histopathology and Dr. Ganji for offering the DC-specific aptamer sequence.

Funding

This work was supported by the research deputy at Mashhad University of Medical Sciences, Mashhad, Iran, under Grant No (981773).

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Authors and Affiliations

  1. Immunology Research Center, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Safoora Pordel, Navideh Haghnavaz, MohammadAli Rezaee, Saeideh Sadat Shobeiri, Bahareh Ansari, Mohammadreza Dashti, Malihe Moghadam, Motahare Khorrami & Mojtaba Sankian

  2. Department of Medical Laboratory Sciences, Faculty of Paramedical, Kurdistan University of Medical Sciences, Sanandaj, Iran

    MohammadAli Rezaee

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Ethics declarations

We declare that some parts of fig. 1, 2, and 3A were drawn using pictures from Servier Medical Art. Servier Medical Art by Servier is licensed under a Creative Commons Attribution 3.0 Unported License (https://creativecommons.org/licenses/by/3.0/). This Figure was modified with text, markings, and annotation using Microsoft Office PowerPoint (version 2010). The first author prepared the graphs (Figs. 3B, 4, 5, and 6) using GraphPad Prism (version 8.4.2, California, USA). Histological photographs were taken with a digital camera (Fig. 7). Scanning electron microscopy (SEM) (MIRA3 TESCAN, Czech Republic) was used to obtain microscopic images of nanoparticles (Fig. 3C).

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Supplementary information

ESM 1

Supplementary 1. gel electrophoresis of DC specific Apt-modified GNPs. Well 1 and 3 were loaded with Apt-modified GNPs and well 2 with naked GNPs (PNG 889 kb)

High resolution image (TIF 2713 kb)

ESM 2

Supplementary 2. SDS-PAGE analysis to evaluate the loaded protein of Pla.orintalis pollen extract on GNPs, well 1: total extract (1000 μg/ml), well 2: 100 μg total extract as control, well 3: non-binding protein of Pla.orintalis pollen extract on GNPs; well 4: detached protein of “Pla. ext-Apts-GNPs” complex, well 5: LMW protein marker (PNG 1352 kb)

High resolution image (TIF 4251 kb)

ESM 3

Supplementary 3. Viability of NIH 3T3 cells and PBMCs treated with different concentrations of GNPs and Apts-GNPs (PNG 165 kb)

High resolution image (TIF 537 kb)

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Pordel, S., Haghnavaz, N., Rezaee, M. et al. An epicutaneous therapeutic pollen-allergen extract delivery system in an allergic rhinitis mouse model: based on allergen loading on DC-specific aptamers conjugated nanogolds. Immunol Res (2023). https://doi.org/10.1007/s12026-023-09445-6

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