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CD38⁺ endothelial remodeling marks spatially patterned vasculopathy in rapidly advancing periodontitis and peri-implantitis

  • Quinn T. Easter
  • , Khoa L.A. Huynh
  • , Camila Schmidt Stolf
  • , Jialiu Xie
  • , Bruno F. Matuck
  • , Akira Hasuike
  • , Zabdiel Alvarado-Martinez
  • , William S. Kim
  • , Zhaoxu Chen
  • , Apoena Aguiar Ribeiro
  • , Nivedita Pareek
  • , Andrea M. Azcarate-Peril
  • , Di Wu
  • , Renato Casarin
  • , Kang I. Ko
  • , Jinze Liu
  • , Kevin M. Byrd
  • Virginia Commonwealth University
  • Universidade Estadual de Campinas
  • University of North Carolina at Chapel Hill
  • Nihon University
  • Independent Contractor
  • University of Pennsylvania
  • University of California at San Francisco

Research output: Contribution to journalArticlepeer-review

Abstract

Oral inflammatory diseases affect nearly half of all humans, yet mechanisms underlying rapidly-destructive inflammation remain poorly understood. We compared peri-implantitis with moderate- and high-grade periodontitis using integrated microbial and single-cell sequencing (>967,169-cells; single-cell RNA-seq, spatial proteotranscriptomics). Laser capture microdissection with compartmental microbiome analysis revealed reduced bacterial load and diversity in peri-implantitis. Expansion of the Human Periodontal Atlas with peri-implantitis single-cell RNA-seq data (36-samples; 121,395 cells) identified CD34+ vascular endothelial cell (VEC) rarefaction and oxidative stress, hypoxia, and NAD⁺ metabolism-associated transcriptional programs enriched in a TNFRSF6B⁺/ICAM1⁺ post-capillary venule (PC-VEC) subpopulation. NAD⁺-consuming ectoenzyme CD38 was selectively enriched and orthogonally confirmed by spatial transcriptomics (6-samples; 283,377-cells) and proteomics (23-samples; 562,397-cells). Spatial neighborhood analyses demonstrated CD38⁺-high PC-VEC expansion, closer proximity, and higher IL16–CD4 T cell signaling in peri-implantitis. Matched high-grade periodontitis biopsies confirmed spatially restricted CD38⁺-VECs despite similar microbial burden, identifying endothelial vasculopathy underlying rapidly advancing oral inflammation and a potential therapeutic axis.

Original languageEnglish
Article number6239
JournalNature Communications
Volume17
Issue number1
DOIs
StatePublished - Dec 2026

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