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      Inflammatory response of gut, spleen, and liver in mice induced by orally administered Porphyromonas gingivalis

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          ABSTRACT

          Background

          Periodontitis is a chronic multifactorial inflammatory disease. Porphyromonas gingivalis is a primary periopathogen in the initiation and development of periodontal disease. Evidence has shown that P. gingivalis is associated with systemic diseases, including IBD and fatty liver disease. Inflammatory response is a key feature of diseases related to this species.

          Methods

          C57BL/6 mice were administered either PBS, or P. gingivalis. After 9 weeks, the inflammatory response in gut, spleen, and liver was analyzed.

          Results

          The findings revealed significant disturbance of the intestinal microbiota and increased inflammatory factors in the gut of P. gingivalis-administered mice. Administrated P. gingivalis remarkably promoted the secretion of IRF-1 and activated the inflammatory pathway IFN-γ/STAT1 in the spleen. Histologically, mice treated with P. gingivalis exhibited hepatocyte damage and lipid deposition. The inflammatory factors IL-17a, IL-6, and ROR-γt were also upregulated in the liver of mice fed with P. gingivalis. Lee’s index, spleen index, and liver index were also increased.

          Conclusion

          These results suggest that administrated P. gingivalis evokes inflammation in gut, spleen, and liver, which might promote the progression of various systemic diseases.

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          Most cited references79

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          Formation of propionate and butyrate by the human colonic microbiota

          The human gut microbiota ferments dietary non-digestible carbohydrates into short-chain fatty acids (SCFA). These microbial products are utilized by the host and propionate and butyrate in particular exert a range of health-promoting functions. Here an overview of the metabolic pathways utilized by gut microbes to produce these two SCFA from dietary carbohydrates and from amino acids resulting from protein breakdown is provided. This overview emphasizes the important role played by cross-feeding of intermediary metabolites (in particular lactate, succinate and 1,2-propanediol) between different gut bacteria. The ecophysiology, including growth requirements and responses to environmental factors, of major propionate and butyrate producing bacteria are discussed in relation to dietary modulation of these metabolites. A detailed understanding of SCFA metabolism by the gut microbiota is necessary to underpin effective strategies to optimize SCFA supply to the host.
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            Periodontal diseases

            The Lancet, 366(9499), 1809-1820
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              The gut–liver axis and the intersection with the microbiome

              In the past decade, an exciting realization has been that diverse liver diseases, ranging from non-alcoholic steatohepatitis, alcoholic steatohepatitis, and cirrhosis, to hepatocellular carcinoma, are not unrelated but fall along a spectrum. Recent work on the biology of the gut-liver communication axis has assisted in understanding the basic biology of both alcoholic and nonalcoholic fatty liver disease. Of immense importance is the massive advancement in understanding of the role of the microbiome, driven by high-throughput DNA sequencing and improved computational techniques that allow the complexity of the microbiome to be interrogated, together with improved experimental designs. Here, we review the gut-liver communications of these various forms of liver disease, explore the molecular, genetic and microbiome relationships, discuss prospects for exploiting the microbiome to determine the stage of liver disease, and to predict the effects of pharmaceutical, dietary, and other interventions at a population and individual level. We conclude that although much remains to be done in understanding the relationship between the microbiome and liver disease, rapid progress towards clinical applications is being made, especially in study designs that complement human intervention studies with mechanistic work in mice that have been humanized in multiple respects, including the genetic, immunological and microbiome characteristics of individual patients. These “avatar mice” may be especially useful for guiding new microbiome-based or microbiome-informed therapies.
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                Author and article information

                Journal
                J Oral Microbiol
                J Oral Microbiol
                Journal of Oral Microbiology
                Taylor & Francis
                2000-2297
                16 June 2022
                2022
                16 June 2022
                : 14
                : 1
                : 2088936
                Affiliations
                [a ]Department of Periodontics, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Diseases; , Shenyang, Liaoning, China
                [b ]Department of Orthodontics, School of Stomatology, China Medical University; , Shenyang, Liaoning, China
                [c ]Department of Stomatology, Lishui University School of Medicine; , Lishui, Zhejing, China
                [d ]Department of Oral Biology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Diseases; , Shenyang, Liaoning, China
                [e ]Department of Stomatology, Science Experiment Center, China Medical University; , Shenyang, Liaoning, China
                Author notes
                CONTACT Yurong Kou yrkou@ 123456cmu.edu.cn No. 117 Nanjing North Street, Heping District, Shenyang, Liaoning Province 110002, China
                Article
                2088936
                10.1080/20002297.2022.2088936
                9225697
                35756539
                77b0a90b-2ff4-4c05-a064-e9ebddcb14fc
                © 2022 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Figures: 6, Tables: 1, References: 79, Pages: 1
                Categories
                Research Article
                Original Article

                Microbiology & Virology
                porphyromonas gingivalis,periodontal disease,intestinal bacteria,inflammation,immune response

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