Periodontal pathogen Aggregatibacter actinomycetemcomitans JP2 correlates with colonic leukocytes decrease and gut microbiome imbalance in mice

IF 3.4 3区医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE

Journal of periodontal research Pub Date : 2024-05-16 DOI:10.1111/jre.13288

André L. A. da Costa, Mariana A. Soares, Talita G. B. Lourenço, Kamila Guimarães-Pinto, Alessandra D. Filardy, Adriana Miranda de Oliveira, Beatriz Gouvêa de Luca, D’ Angelo Carlo Magliano, Olga M. O. Araujo, Larissa Moura, Ricardo Tadeu Lopes, Ana Luisa Palhares de Miranda, Jorge L. M. Tributino, Ana Paula Vieira Colombo

{"title":"Periodontal pathogen Aggregatibacter actinomycetemcomitans JP2 correlates with colonic leukocytes decrease and gut microbiome imbalance in mice","authors":"André L. A. da Costa, Mariana A. Soares, Talita G. B. Lourenço, Kamila Guimarães-Pinto, Alessandra D. Filardy, Adriana Miranda de Oliveira, Beatriz Gouvêa de Luca, D’ Angelo Carlo Magliano, Olga M. O. Araujo, Larissa Moura, Ricardo Tadeu Lopes, Ana Luisa Palhares de Miranda, Jorge L. M. Tributino, Ana Paula Vieira Colombo","doi":"10.1111/jre.13288","DOIUrl":null,"url":null,"abstract":"<div>\n \n \n <section>\n \n <h3> Aim</h3>\n \n <p>Evidence suggests that translocation of oral pathogens through the oral–gut axis may induce intestinal dysbiosis. This study aimed to evaluate the impact of a highly leukotoxic <i>Aggregatibacter actinomycetemcomitans</i> (<i>Aa</i>) strain on the gut microbiota, intestinal mucosal integrity and immune system in healthy mice.</p>\n </section>\n \n <section>\n \n <h3> Methods</h3>\n \n <p>Eight-week-old male C57BL6 mice were divided into control (<i>n</i> = 16) and JP2 groups (<i>n</i> = 19), which received intragastric gavage with PBS and with a suspension of <i>Aa</i> JP2 (HK921), respectively, twice a week for 4 weeks. Colonic <i>lamina propria</i>, fecal material, serum, gingival tissues, and mandibles were obtained for analyses of leukocyte populations, inflammatory mediators, mucosal integrity, alveolar bone loss, and gut microbiota. Differences between groups for these parameters were examined by non-parametric tests.</p>\n </section>\n \n <section>\n \n <h3> Results</h3>\n \n <p>The gut microbial richness and the number of colonic macrophages, neutrophils, and monocytes were significantly lower in <i>Aa</i> JP2-infected mice than in controls (<i>p</i> < .05). In contrast, infected animals showed higher abundance of <i>Clostridiaceae, Lactobacillus taiwanensis, Helicobacter rodentium</i>, higher levels of IL-6 expression in colonic tissues, and higher splenic MPO activity than controls (<i>p</i> < .05). No differences in tight junction expression, serum endotoxin levels, and colonic inflammatory cytokines were observed between groups. Infected animals presented also slightly more alveolar bone loss and gingival IL-6 levels than controls (<i>p</i> < .05).</p>\n </section>\n \n <section>\n \n <h3> Conclusion</h3>\n \n <p>Based on this model, intragastric administration of <i>Aa</i> JP2 is associated with changes in the gut ecosystem of healthy hosts, characterized by less live/recruited myeloid cells, enrichment of the gut microbiota with pathobionts and decrease in commensals. Negligible levels of colonic pro-inflammatory cytokines, and no signs of mucosal barrier disruption were related to these changes.</p>\n </section>\n </div>","PeriodicalId":16715,"journal":{"name":"Journal of periodontal research","volume":"59 5","pages":"961-973"},"PeriodicalIF":3.4000,"publicationDate":"2024-05-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of periodontal research","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/jre.13288","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"DENTISTRY, ORAL SURGERY & MEDICINE","Score":null,"Total":0}

引用次数: 0

Abstract

Aim

Evidence suggests that translocation of oral pathogens through the oral–gut axis may induce intestinal dysbiosis. This study aimed to evaluate the impact of a highly leukotoxic Aggregatibacter actinomycetemcomitans (Aa) strain on the gut microbiota, intestinal mucosal integrity and immune system in healthy mice.

Methods

Eight-week-old male C57BL6 mice were divided into control (n = 16) and JP2 groups (n = 19), which received intragastric gavage with PBS and with a suspension of Aa JP2 (HK921), respectively, twice a week for 4 weeks. Colonic lamina propria, fecal material, serum, gingival tissues, and mandibles were obtained for analyses of leukocyte populations, inflammatory mediators, mucosal integrity, alveolar bone loss, and gut microbiota. Differences between groups for these parameters were examined by non-parametric tests.

Results

The gut microbial richness and the number of colonic macrophages, neutrophils, and monocytes were significantly lower in Aa JP2-infected mice than in controls (p < .05). In contrast, infected animals showed higher abundance of Clostridiaceae, Lactobacillus taiwanensis, Helicobacter rodentium, higher levels of IL-6 expression in colonic tissues, and higher splenic MPO activity than controls (p < .05). No differences in tight junction expression, serum endotoxin levels, and colonic inflammatory cytokines were observed between groups. Infected animals presented also slightly more alveolar bone loss and gingival IL-6 levels than controls (p < .05).

Conclusion

Based on this model, intragastric administration of Aa JP2 is associated with changes in the gut ecosystem of healthy hosts, characterized by less live/recruited myeloid cells, enrichment of the gut microbiota with pathobionts and decrease in commensals. Negligible levels of colonic pro-inflammatory cytokines, and no signs of mucosal barrier disruption were related to these changes.

Abstract Image

查看原文本刊更多论文

牙周病原体放线杆菌 JP2 与小鼠结肠白细胞减少和肠道微生物群失衡有关。

目的：有证据表明，口腔病原体通过口腔-肠道轴转运可能会诱发肠道菌群失调。本研究旨在评估高白细胞毒性放线菌（Aa）菌株对健康小鼠肠道微生物群、肠道粘膜完整性和免疫系统的影响：将八周大的雄性 C57BL6 小鼠分为对照组（n = 16）和 JP2 组（n = 19），分别灌胃 PBS 和 Aa JP2（HK921）悬浮液，每周两次，连续 4 周。采集结肠固有层、粪便、血清、牙龈组织和下颌骨，用于分析白细胞群、炎症介质、粘膜完整性、牙槽骨损失和肠道微生物群。这些参数的组间差异通过非参数检验进行检验：结果：Aa JP2 感染小鼠的肠道微生物丰富度以及结肠巨噬细胞、中性粒细胞和单核细胞的数量均显著低于对照组（p 结论：Aa JP2 感染小鼠的肠道微生物丰富度和结肠巨噬细胞、中性粒细胞和单核细胞的数量均显著低于对照组（p）：根据这一模型，胃内注射 Aa JP2 与健康宿主肠道生态系统的变化有关，其特点是活的/招募的髓样细胞减少，肠道微生物群中病原菌增多，共生菌减少。这些变化与结肠促炎细胞因子的水平微不足道，也没有粘膜屏障破坏的迹象。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Journal of periodontal research 医学-牙科与口腔外科

CiteScore

6.90

自引率

5.70%

发文量

103

审稿时长

6-12 weeks

期刊介绍： The Journal of Periodontal Research is an international research periodical the purpose of which is to publish original clinical and basic investigations and review articles concerned with every aspect of periodontology and related sciences. Brief communications (1-3 journal pages) are also accepted and a special effort is made to ensure their rapid publication. Reports of scientific meetings in periodontology and related fields are also published. One volume of six issues is published annually.