The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment

Abstract Background In a pilot study, we found that feces transplantation from elderly individuals to mice significantly caused cognitive impairment. Paenalcaligenes hominis and Escherichia coli are increasingly detected in the feces of elderly adults and aged mice. Therefore, we isolated Paenalcali...

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Main Authors: Kyung-Eon Lee, Jeon-Kyung Kim, Sang-Kap Han, Dong Yun Lee, Hae-Ji Lee, Sung-Vin Yim, Dong-Hyun Kim
Format: Article
Language:English
Published: BMC 2020-07-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-020-00881-2
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spelling doaj-a948abf9186148bf983831f0efc5319e2020-11-25T03:02:55ZengBMCMicrobiome2049-26182020-07-018111810.1186/s40168-020-00881-2The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairmentKyung-Eon Lee0Jeon-Kyung Kim1Sang-Kap Han2Dong Yun Lee3Hae-Ji Lee4Sung-Vin Yim5Dong-Hyun Kim6Neurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee UniversityDepartment of Clinical Pharmacology and Therapeutics, College of Medicine, Kyung Hee UniversityNeurobiota Research Center, Department of Life and Nanopharmaceutical Sciences, College of Pharmacy, Kyung Hee UniversityAbstract Background In a pilot study, we found that feces transplantation from elderly individuals to mice significantly caused cognitive impairment. Paenalcaligenes hominis and Escherichia coli are increasingly detected in the feces of elderly adults and aged mice. Therefore, we isolated Paenalcaligenes hominis and Escherichia coli from the feces of elderly individuals and aged mice and examined their effects on the occurrence of age-related degenerative cognitive impairment and colonic inflammation in mice. Results The transplantation of feces collected from elderly people and aged mice caused significantly more severe cognitive impairment in transplanted young mice than those from young adults and mice. Oral gavage of Paenalcaligenes hominis caused strong cognitive impairment and colitis in specific pathogen-free (SPF) and germ-free mice. Escherichia coli also induced cognitive impairment and colitis in SPF mice. Oral gavage of Paenalcaligenes hominis, its extracellular vesicles (EVs), and/or lipopolysaccharide caused cognitive impairment and colitis in mice. However, celiac vagotomy significantly inhibited the occurrence of cognitive impairment, but not colitis, in mice exposed to Paenalcaligenes hominis or its EVs, whereas its lipopolysaccharide or Escherichia coli had no such effects. Vagotomy also inhibited the infiltration of EVs into the hippocampus. Conclusions Paenalcaligenes hominis, particularly its EVs, can cause cognitive function-impaired disorders, such as Alzheimer’s disease, and its EVs may penetrate the brain through the blood as well as the vagus nerve. Video Abstracthttp://link.springer.com/article/10.1186/s40168-020-00881-2Paenalcaligenes hominisExtracellular vesicleLipopolysaccharideCognitive declineColitis
collection DOAJ
language English
format Article
sources DOAJ
author Kyung-Eon Lee
Jeon-Kyung Kim
Sang-Kap Han
Dong Yun Lee
Hae-Ji Lee
Sung-Vin Yim
Dong-Hyun Kim
spellingShingle Kyung-Eon Lee
Jeon-Kyung Kim
Sang-Kap Han
Dong Yun Lee
Hae-Ji Lee
Sung-Vin Yim
Dong-Hyun Kim
The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment
Microbiome
Paenalcaligenes hominis
Extracellular vesicle
Lipopolysaccharide
Cognitive decline
Colitis
author_facet Kyung-Eon Lee
Jeon-Kyung Kim
Sang-Kap Han
Dong Yun Lee
Hae-Ji Lee
Sung-Vin Yim
Dong-Hyun Kim
author_sort Kyung-Eon Lee
title The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment
title_short The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment
title_full The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment
title_fullStr The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment
title_full_unstemmed The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment
title_sort extracellular vesicle of gut microbial paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2020-07-01
description Abstract Background In a pilot study, we found that feces transplantation from elderly individuals to mice significantly caused cognitive impairment. Paenalcaligenes hominis and Escherichia coli are increasingly detected in the feces of elderly adults and aged mice. Therefore, we isolated Paenalcaligenes hominis and Escherichia coli from the feces of elderly individuals and aged mice and examined their effects on the occurrence of age-related degenerative cognitive impairment and colonic inflammation in mice. Results The transplantation of feces collected from elderly people and aged mice caused significantly more severe cognitive impairment in transplanted young mice than those from young adults and mice. Oral gavage of Paenalcaligenes hominis caused strong cognitive impairment and colitis in specific pathogen-free (SPF) and germ-free mice. Escherichia coli also induced cognitive impairment and colitis in SPF mice. Oral gavage of Paenalcaligenes hominis, its extracellular vesicles (EVs), and/or lipopolysaccharide caused cognitive impairment and colitis in mice. However, celiac vagotomy significantly inhibited the occurrence of cognitive impairment, but not colitis, in mice exposed to Paenalcaligenes hominis or its EVs, whereas its lipopolysaccharide or Escherichia coli had no such effects. Vagotomy also inhibited the infiltration of EVs into the hippocampus. Conclusions Paenalcaligenes hominis, particularly its EVs, can cause cognitive function-impaired disorders, such as Alzheimer’s disease, and its EVs may penetrate the brain through the blood as well as the vagus nerve. Video Abstract
topic Paenalcaligenes hominis
Extracellular vesicle
Lipopolysaccharide
Cognitive decline
Colitis
url http://link.springer.com/article/10.1186/s40168-020-00881-2
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