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Pangolin scales as adaptations for innate immunity against pathogens

Lookup NU author(s): Professor Nicholas JakubovicsORCiD

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This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND).


Abstract

© The Author(s) 2024.Background: Pangolins are the only mammals that have overlapping scales covering most of their bodies, and they play a crucial role in the ecosystem, biological research, and human health and disease. Previous studies indicated pangolin scale might provide an important mechanical defense to themselves. The origin and exact functions of this unique trait remain a mystery. Using a multi-omics analysis approach, we report a novel functional explanation for how mammalian scales can provide host–pathogen defense. Results: Our data suggest that pangolin scales have a sophisticated structure that could potentially trap pathogens. We identified numerous proteins and metabolites exhibiting antimicrobial activity, which could suggest a role for scales in pathogen defense. Notably, we found evidence suggesting the presence of exosomes derived from diverse cellular origins, including mesenchymal stem cells, immune cells, and keratinocytes. This observation suggests a complex interplay where various cell types may contribute to the release of exosomes and antimicrobial compounds at the interface between scales and viable tissue. These findings indicate that pangolin scales may serve as a multifaceted defense system, potentially contributing to innate immunity. Comparisons with human nail and hair revealed pangolin-specific proteins that were enriched in functions relating to sensing, immune responses, neutrophil degranulation, and stress responses. We demonstrated the antimicrobial activity of key pangolin scale components on pathogenic bacteria by antimicrobial assays. Conclusions: This study identifies a potential role of pangolin scales and implicates scales, as possible determinants of pathogen defense due to their structure and contents. We indicate for the first time the presence of exosomes in pangolin scales and propose the new functions of scales and their mechanisms. This new mechanism could have implications for multiple fields, including providing interesting new research directions and important insights that can be useful for synthesizing and implementing new biomimetic antimicrobial approaches.


Publication metadata

Author(s): Tian X, Chen L, Zhou J, Wang E, Wang M, Jakubovics N, Li J, Song K, Lau KT, Koepfli K-P, Zhang S, Tan GYA, Yang Y, Choo SW

Publication type: Article

Publication status: Published

Journal: BMC Biology

Year: 2024

Volume: 22

Issue: 1

Online publication date: 14/10/2024

Acceptance date: 04/10/2024

Date deposited: 28/10/2024

ISSN (electronic): 1741-7007

Publisher: BioMed Central Ltd

URL: https://doi.org/10.1186/s12915-024-02034-5

DOI: 10.1186/s12915-024-02034-5

Data Access Statement: The sequencing data in this study have been deposited in the NCBI Sequence Read Archive (SRA) under Bioproject accession number PRJNA1155658 [68]. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the PRIDE partner repository [69] with dataset identifier PXD052288 [70]. The Supplementary Figures, Supplementary Tables, Supplementary Methods, and Original Data are presented as Additional file A, Additional file B, Additional file C, and Additional file D, respectively, and can be accessed online via Figshare (https://figshare.com/) at the following DOI: https://doi.org/https://doi.org/10.6084/m9.figshare.26889598 [71]. Data supporting the findings of this study are included in the published paper and additional information.

PubMed id: 39397000


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Funding

Funder referenceFunder name
5000105
WB20210429000008
Wenzhou Municipal Key Laboratory for Applied Biomedical and the Biopharmaceutical Informatics
WB20211227000125
Wenzhou-Kean University
Zhejiang Bioinformatics International Science and Technology Cooperation Center at Wenzhou-Kean University

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