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

Author

Listed:
  • 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
    Nihon University School of Dentistry)

  • 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
    University of Florida)

  • Inês Sequeira

    (Queen Mary University of London)

  • Hyun Koo

    (University of Pennsylvania)

  • Katarzyna M. Tyc

    (Virginia Commonwealth University
    Virginia Commonwealth University)

  • Jinze Liu

    (Virginia Commonwealth University
    Virginia Commonwealth University)

  • Kang I. Ko

    (University of Pennsylvania)

  • Sarah A. Teichmann

    (Wellcome Genome Campus
    Cavendish Laboratory)

  • Kevin M. Byrd

    (ADA Science & Research Institute
    National Institutes of Health
    University of North Carolina at Chapel Hill)

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.

Suggested Citation

  • 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 , 2024. "Single-cell and spatially resolved interactomics of tooth-associated keratinocytes in periodontitis," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49037-y
    DOI: 10.1038/s41467-024-49037-y
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