Single-cell and spatially resolved interactomics of tooth-associated keratinocytes in periodontitis

Quinn T. Easter, Bruno Fernandes Matuck, Germán Beldorati Stark, Catherine L. Worth, Alexander V. Predeus, Brayon Fremin, Khoa Huynh, Vaishnavi Ranganathan, Zhi Ren, Diana Pereira, Brittany T. Rupp, Theresa Weaver, Kathryn Miller, Paola Perez, Akira Hasuike, Zhaoxu Chen, Mandy Bush, Xufeng Qu, Janice Lee, Scott H. Randell, Shannon M. Wallet, Inês Sequeira, Hyun Koo, Katarzyna M. Tyc, Jinze Liu, Kang I. Ko, Sarah A. Teichmann and Kevin M. Byrd ()
Additional contact information
Quinn T. Easter: ADA Science & Research Institute
Bruno Fernandes Matuck: ADA Science & Research Institute
Germán Beldorati Stark: Parse Biosciences
Catherine L. Worth: The Bioinformatics CRO
Alexander V. Predeus: Wellcome Genome Campus
Brayon Fremin: The Bioinformatics CRO
Khoa Huynh: Virginia Commonwealth University
Vaishnavi Ranganathan: Carnegie Mellon University
Zhi Ren: University of Pennsylvania
Diana Pereira: Queen Mary University of London
Brittany T. Rupp: ADA Science & Research Institute
Theresa Weaver: ADA Science & Research Institute
Kathryn Miller: Akoya Biosciences Inc.
Paola Perez: National Institutes of Health
Akira Hasuike: ADA Science & Research Institute
Zhaoxu Chen: University of Pennsylvania
Mandy Bush: University of North Carolina at Chapel Hill
Xufeng Qu: Virginia Commonwealth University
Janice Lee: National Institutes of Health
Scott H. Randell: University of North Carolina at Chapel Hill
Shannon M. Wallet: University of North Carolina at Chapel Hill
Inês Sequeira: Queen Mary University of London
Hyun Koo: University of Pennsylvania
Katarzyna M. Tyc: Virginia Commonwealth University
Jinze Liu: Virginia Commonwealth University
Kang I. Ko: University of Pennsylvania
Sarah A. Teichmann: Wellcome Genome Campus
Kevin M. Byrd: ADA Science & Research Institute

Nature Communications, 2024, vol. 15, issue 1, 1-23

Abstract: Abstract Periodontitis affects billions of people worldwide. To address relationships of periodontal niche cell types and microbes in periodontitis, we generated an integrated single-cell RNA sequencing (scRNAseq) atlas of human periodontium (34-sample, 105918-cell), including sulcular and junctional keratinocytes (SK/JKs). SK/JKs displayed altered differentiation states and were enriched for effector cytokines in periodontitis. Single-cell metagenomics revealed 37 bacterial species with cell-specific tropism. Fluorescence in situ hybridization detected intracellular 16 S and mRNA signals of multiple species and correlated with SK/JK proinflammatory phenotypes in situ. Cell-cell communication analysis predicted keratinocyte-specific innate and adaptive immune interactions. Highly multiplexed immunofluorescence (33-antibody) revealed peri-epithelial immune foci, with innate cells often spatially constrained around JKs. Spatial phenotyping revealed immunosuppressed JK-microniches and SK-localized tertiary lymphoid structures in periodontitis. Here, we demonstrate impacts on and predicted interactomics of SK and JK cells in health and periodontitis, which requires further investigation to support precision periodontal interventions in states of chronic inflammation.

Date: 2024
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DOI: 10.1038/s41467-024-49037-y

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