Periodontal ligament tissues support neutrophil differentiation and maturation processes

IntroductionPeriodontal ligament is the soft connective tissue joining the roots of teeth with alveolar bone. The periodontal ligament presents significant cellular heterogeneity, including fibroblasts, endothelial cells, cementoblasts, osteoblasts, osteoclasts, and immune cells such as macrophages...

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Main Authors: Guillermo Villagómez-Olea, Eileen Uribe-Querol, Francisco Javier Marichi-Rodríguez, Jorge Meléndez-Zajgla, Marco Antonio Alvaréz-Pérez, Carlos Rosales
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2024.1446541/full
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author Guillermo Villagómez-Olea
Eileen Uribe-Querol
Francisco Javier Marichi-Rodríguez
Jorge Meléndez-Zajgla
Marco Antonio Alvaréz-Pérez
Carlos Rosales
author_facet Guillermo Villagómez-Olea
Eileen Uribe-Querol
Francisco Javier Marichi-Rodríguez
Jorge Meléndez-Zajgla
Marco Antonio Alvaréz-Pérez
Carlos Rosales
author_sort Guillermo Villagómez-Olea
collection DOAJ
description IntroductionPeriodontal ligament is the soft connective tissue joining the roots of teeth with alveolar bone. The periodontal ligament presents significant cellular heterogeneity, including fibroblasts, endothelial cells, cementoblasts, osteoblasts, osteoclasts, and immune cells such as macrophages and neutrophils. These cells have crucial roles for periodontium homeostasis and function. However, certain cell types, such as neutrophils, remain poorly characterized in this tissue, despite their natural abundance and relevance in processes and diseases affecting the periodontal ligament.MethodsIn order to characterize neutrophils present in periodontal ligament, and get some insight into their functions, single-cell RNA sequencing data from published reports was analyzed to integrate and create a comprehensive map of neutrophil heterogeneity within the murine periodontal ligament under steady-state conditions.ResultsFour distinct neutrophil populations were identified based on their unique transcriptional signatures. Comparison and trajectory analysis revealed that these populations represent discrete stages of neutrophils undergoing maturation. These neutrophil populations were also classified, based on their granule content-associated signatures, as azurophil, specific, a transitional stage between specific and gelatinase (specific/gelatinase), and gelatinase. This reflects the sequential order of granule formation during neutrophil development (granulopoiesis) in the bone marrow.DiscussionTogether, our findings indicate that the periodontal ligament may serve as a microenvironment where the ordered and sequential maturation of neutrophils takes place. This suggests that similarly to other niches, the murine periodontal ligament can support, to some extent, hematopoietic processes such as granulopoiesis.
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spelling doaj-art-a6803854b45441a8adbafbf36f44599c2024-11-11T11:12:59ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-11-011510.3389/fimmu.2024.14465411446541Periodontal ligament tissues support neutrophil differentiation and maturation processesGuillermo Villagómez-Olea0Eileen Uribe-Querol1Francisco Javier Marichi-Rodríguez2Jorge Meléndez-Zajgla3Marco Antonio Alvaréz-Pérez4Carlos Rosales5Laboratorio de Bioingeniería de Tejidos, División de Estudios de Posgrado e Investigación, Facultad de Odontología, Universidad Nacional Autónoma de México, Mexico City, MexicoLaboratorio de Biología del Desarrollo, División de Estudios de Posgrado e Investigación, Facultad de Odontología, Universidad Nacional Autónoma de México, Mexico City, MexicoDepartamento de Ortodoncia, División de Estudios de Posgrado e Investigación, Facultad de Odontología, Universidad Nacional Autónoma de México, Mexico City, MexicoLaboratorio de Genómica Funcional, Instituto Nacional de Medicina Genómica, Mexico City, MexicoLaboratorio de Bioingeniería de Tejidos, División de Estudios de Posgrado e Investigación, Facultad de Odontología, Universidad Nacional Autónoma de México, Mexico City, MexicoDepartamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Mexico City, MexicoIntroductionPeriodontal ligament is the soft connective tissue joining the roots of teeth with alveolar bone. The periodontal ligament presents significant cellular heterogeneity, including fibroblasts, endothelial cells, cementoblasts, osteoblasts, osteoclasts, and immune cells such as macrophages and neutrophils. These cells have crucial roles for periodontium homeostasis and function. However, certain cell types, such as neutrophils, remain poorly characterized in this tissue, despite their natural abundance and relevance in processes and diseases affecting the periodontal ligament.MethodsIn order to characterize neutrophils present in periodontal ligament, and get some insight into their functions, single-cell RNA sequencing data from published reports was analyzed to integrate and create a comprehensive map of neutrophil heterogeneity within the murine periodontal ligament under steady-state conditions.ResultsFour distinct neutrophil populations were identified based on their unique transcriptional signatures. Comparison and trajectory analysis revealed that these populations represent discrete stages of neutrophils undergoing maturation. These neutrophil populations were also classified, based on their granule content-associated signatures, as azurophil, specific, a transitional stage between specific and gelatinase (specific/gelatinase), and gelatinase. This reflects the sequential order of granule formation during neutrophil development (granulopoiesis) in the bone marrow.DiscussionTogether, our findings indicate that the periodontal ligament may serve as a microenvironment where the ordered and sequential maturation of neutrophils takes place. This suggests that similarly to other niches, the murine periodontal ligament can support, to some extent, hematopoietic processes such as granulopoiesis.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1446541/fullneutrophilperiodontiumperiodontal ligamentinflammationgranulopoiesissingle-cell RNA sequencing
spellingShingle Guillermo Villagómez-Olea
Eileen Uribe-Querol
Francisco Javier Marichi-Rodríguez
Jorge Meléndez-Zajgla
Marco Antonio Alvaréz-Pérez
Carlos Rosales
Periodontal ligament tissues support neutrophil differentiation and maturation processes
Frontiers in Immunology
neutrophil
periodontium
periodontal ligament
inflammation
granulopoiesis
single-cell RNA sequencing
title Periodontal ligament tissues support neutrophil differentiation and maturation processes
title_full Periodontal ligament tissues support neutrophil differentiation and maturation processes
title_fullStr Periodontal ligament tissues support neutrophil differentiation and maturation processes
title_full_unstemmed Periodontal ligament tissues support neutrophil differentiation and maturation processes
title_short Periodontal ligament tissues support neutrophil differentiation and maturation processes
title_sort periodontal ligament tissues support neutrophil differentiation and maturation processes
topic neutrophil
periodontium
periodontal ligament
inflammation
granulopoiesis
single-cell RNA sequencing
url https://www.frontiersin.org/articles/10.3389/fimmu.2024.1446541/full
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