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Oral Porphyromonas gingivalis infection affects intestinal microbiota and promotes atherosclerosis

Authors
 Sowon Park  ;  Inyoung Kim  ;  Soo Jung Han  ;  Soyeon Kwon  ;  Eun-Ji Min  ;  Wonkyoung Cho  ;  Hong Koh  ;  Bon-Nyeo Koo  ;  Jung Seok Lee  ;  Jae-Sung Kwon  ;  Kyoung Yul Seo  ;  Jong-Won Ha  ;  Young Mi Park 
Citation
 JOURNAL OF CLINICAL PERIODONTOLOGY, Vol.50(11) : 1553-1567, 2023-11 
Journal Title
JOURNAL OF CLINICAL PERIODONTOLOGY
ISSN
 0303-6979 
Issue Date
2023-11
Keywords
Porphyromonas gingivalis ; atherosclerosis ; intestinal dysbiosis ; microbiota
Abstract
Aim: The link between periodontitis and intestinal dysbiosis, two factors that contribute to atherosclerosis, has not been clearly defined. We investigated the integrative effects of oral infection with Porphyromonas gingivalis (PG), the major pathogen for periodontitis, on intestinal microbiota and atherosclerosis.

Materials and methods: ApoE-/- mice were fed a normal chow diet (NC), a Western diet (WD) or a WD with oral PG infection (PG). The PG infection was investigated by placing a total of 109 CFUs of live PG into the oral cavity of each mouse using a feeding needle five times a week for 3 weeks. Atherosclerotic lesions of the aortae were measured, and blood lipoproteins and the expression of molecules related to lipid metabolism in the liver were analysed. We also performed 16S RNA sequencing and a microbiome analysis using faeces.

Results: En face bloc preparation of the aortae showed that the PG group had a 1.7-fold increase in atherosclerotic lesions compared with the WD group (p < .01). Serum analyses showed that oral PG infection induced a significant decrease in high-density lipoprotein (HDL) and triglyceride. Western blots of hepatic tissue lysates revealed that PG infection reduced the expression of scavenger receptor class B type 1 (SR-B1) in the liver by 50%. Faecal microbiota analysis revealed that species richness estimates (Chao1, ACE) decreased immediately after PG infection. PG infection also induced a significant decrease in Shannon diversity and an increase in Simpson's indices in the WD-fed mice. PG infection significantly increased the phyla Actinobacteria and Deferribacteres, along with the species Mucispirillum schaedleri and Lactobacillus gasseri, in the mice. The functional study showed that PG infection increased the expression of proteins that function in carbohydrate and glucose metabolism, including phosphotransferase system (PTS) proteins and the GntR family transcriptional regulator.

Conclusions: Oral PG infection promotes atherosclerosis and induces significant metabolic changes, including reduced serum HDL and reduced hepatic SR-B1 and ABCA1 expression, as well as changes in intestinal microbiota. Our study suggests that intestinal dysbiosis accompanies periodontitis and could play a role in atherosclerosis.
Full Text
https://onlinelibrary.wiley.com/doi/10.1111/jcpe.13864
DOI
10.1111/jcpe.13864
Appears in Collections:
1. College of Medicine (의과대학) > Dept. of Anesthesiology and Pain Medicine (마취통증의학교실) > 1. Journal Papers
1. College of Medicine (의과대학) > Dept. of Internal Medicine (내과학교실) > 1. Journal Papers
1. College of Medicine (의과대학) > Dept. of Ophthalmology (안과학교실) > 1. Journal Papers
1. College of Medicine (의과대학) > Dept. of Pediatrics (소아과학교실) > 1. Journal Papers
2. College of Dentistry (치과대학) > Dept. of Dental Biomaterials and Bioengineering (치과생체재료공학교실) > 1. Journal Papers
2. College of Dentistry (치과대학) > Dept. of Periodontics (치주과학교실) > 1. Journal Papers
Yonsei Authors
Koh, Hong(고홍) ORCID logo https://orcid.org/0000-0002-3660-7483
Koo, Bon-Nyeo(구본녀) ORCID logo https://orcid.org/0000-0002-3189-1673
Kwon, Jae-Sung(권재성) ORCID logo https://orcid.org/0000-0001-9803-7730
Park, So Won(박소원) ORCID logo https://orcid.org/0000-0002-2498-8004
Seo, Kyoung Yul(서경률) ORCID logo https://orcid.org/0000-0002-9855-1980
Lee, Jung Seok(이중석) ORCID logo https://orcid.org/0000-0003-1276-5978
Ha, Jong Won(하종원) ORCID logo https://orcid.org/0000-0002-8260-2958
URI
https://ir.ymlib.yonsei.ac.kr/handle/22282913/196639
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