Impairment of spermatogenesis and sperm motility by the high-fat diet-induced dysbiosis of gut microbes

ObjectiveHigh-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can functionally influence spermatogenesis and sperm motility.DesignFaecal microbes derived from the HFD-fed or normal diet (ND)-fed male mice...

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Published in	Gut Vol. 69; no. 9; pp. 1608 - 1619
Main Authors	Ding, Ning, Zhang, Xin, Zhang, Xue Di, Jing, Jun, Liu, Shan Shan, Mu, Yun Ping, Peng, Li Li, Yan, Yun Jing, Xiao, Geng Miao, Bi, Xin Yun, Chen, Hao, Li, Fang Hong, Yao, Bing, Zhao, Allan Z
Format	Journal Article
Language	English
Published	England BMJ Publishing Group Ltd and British Society of Gastroenterology 01.09.2020 BMJ Publishing Group LTD BMJ Publishing Group
Series	Original research
Subjects	Animals Antibodies Bacteroides Bacteroides - isolation & purification Chronic illnesses Correlation of Data Cytokines Cytokines - analysis Deoxyribonucleic acid Diabetes Diet Diet, High-Fat - adverse effects Digestive system DNA Dysbacteriosis Dysbiosis - etiology Dysbiosis - microbiology Endotoxemia - microbiology endotoxin Epididymis Epididymis - immunology Epididymis - pathology Feces - microbiology Gastric motility Gastrointestinal Microbiome - immunology Gastrointestinal tract Gene expression Glucose Gut Microbiota High fat diet Humans Infertility Inflammation intestinal microbiology Intestinal microflora Intestine Lymphocytes T Macrophages Macrophages - immunology Male Meiosis Metabolic disorders Mice Microbiota Microorganisms Mitochondria Motility Obesity Prevotella Prevotella - isolation & purification Ribonucleic acid RNA Sperm Sperm Motility - immunology Spermatogenesis Spermatogenesis - immunology T-Lymphocytes - immunology Testes Transplantation China intestinal microbiology diet inflammation endotoxin
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Abstract	ObjectiveHigh-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can functionally influence spermatogenesis and sperm motility.DesignFaecal microbes derived from the HFD-fed or normal diet (ND)-fed male mice were transplanted to the mice maintained on ND. The gut microbes, sperm count and motility were analysed. Human faecal/semen/blood samples were collected to assess microbiota, sperm quality and endotoxin.ResultsTransplantation of the HFD gut microbes into the ND-maintained (HFD-FMT) mice resulted in a significant decrease in spermatogenesis and sperm motility, whereas similar transplantation with the microbes from the ND-fed mice failed to do so. Analysis of the microbiota showed a profound increase in genus Bacteroides and Prevotella, both of which likely contributed to the metabolic endotoxaemia in the HFD-FMT mice. Interestingly, the gut microbes from clinical subjects revealed a strong negative correlation between the abundance of Bacteroides-Prevotella and sperm motility, and a positive correlation between blood endotoxin and Bacteroides abundance. Transplantation with HFD microbes also led to intestinal infiltration of T cells and macrophages as well as a significant increase of pro-inflammatory cytokines in the epididymis, suggesting that epididymal inflammation have likely contributed to the impairment of sperm motility. RNA-sequencing revealed significant reduction in the expression of those genes involved in gamete meiosis and testicular mitochondrial functions in the HFD-FMT mice.ConclusionWe revealed an intimate linkage between HFD-induced microbiota dysbiosis and defect in spermatogenesis with elevated endotoxin, dysregulation of testicular gene expression and localised epididymal inflammation as the potential causes.Trial registration number NCT03634644.
AbstractList	ObjectiveHigh-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can functionally influence spermatogenesis and sperm motility.DesignFaecal microbes derived from the HFD-fed or normal diet (ND)-fed male mice were transplanted to the mice maintained on ND. The gut microbes, sperm count and motility were analysed. Human faecal/semen/blood samples were collected to assess microbiota, sperm quality and endotoxin.ResultsTransplantation of the HFD gut microbes into the ND-maintained (HFD-FMT) mice resulted in a significant decrease in spermatogenesis and sperm motility, whereas similar transplantation with the microbes from the ND-fed mice failed to do so. Analysis of the microbiota showed a profound increase in genus Bacteroides and Prevotella, both of which likely contributed to the metabolic endotoxaemia in the HFD-FMT mice. Interestingly, the gut microbes from clinical subjects revealed a strong negative correlation between the abundance of Bacteroides-Prevotella and sperm motility, and a positive correlation between blood endotoxin and Bacteroides abundance. Transplantation with HFD microbes also led to intestinal infiltration of T cells and macrophages as well as a significant increase of pro-inflammatory cytokines in the epididymis, suggesting that epididymal inflammation have likely contributed to the impairment of sperm motility. RNA-sequencing revealed significant reduction in the expression of those genes involved in gamete meiosis and testicular mitochondrial functions in the HFD-FMT mice.ConclusionWe revealed an intimate linkage between HFD-induced microbiota dysbiosis and defect in spermatogenesis with elevated endotoxin, dysregulation of testicular gene expression and localised epididymal inflammation as the potential causes.Trial registration number NCT03634644. High-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can functionally influence spermatogenesis and sperm motility. Faecal microbes derived from the HFD-fed or normal diet (ND)-fed male mice were transplanted to the mice maintained on ND. The gut microbes, sperm count and motility were analysed. Human faecal/semen/blood samples were collected to assess microbiota, sperm quality and endotoxin. Transplantation of the HFD gut microbes into the ND-maintained (HFD-FMT) mice resulted in a significant decrease in spermatogenesis and sperm motility, whereas similar transplantation with the microbes from the ND-fed mice failed to do so. Analysis of the microbiota showed a profound increase in genus and , both of which likely contributed to the metabolic endotoxaemia in the HFD-FMT mice. Interestingly, the gut microbes from clinical subjects revealed a strong negative correlation between the abundance of and sperm motility, and a positive correlation between blood endotoxin and abundance. Transplantation with HFD microbes also led to intestinal infiltration of T cells and macrophages as well as a significant increase of pro-inflammatory cytokines in the epididymis, suggesting that epididymal inflammation have likely contributed to the impairment of sperm motility. RNA-sequencing revealed significant reduction in the expression of those genes involved in gamete meiosis and testicular mitochondrial functions in the HFD-FMT mice. We revealed an intimate linkage between HFD-induced microbiota dysbiosis and defect in spermatogenesis with elevated endotoxin, dysregulation of testicular gene expression and localised epididymal inflammation as the potential causes. NCT03634644. ObjectiveHigh-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can functionally influence spermatogenesis and sperm motility.DesignFaecal microbes derived from the HFD-fed or normal diet (ND)-fed male mice were transplanted to the mice maintained on ND. The gut microbes, sperm count and motility were analysed. Human faecal/semen/blood samples were collected to assess microbiota, sperm quality and endotoxin.ResultsTransplantation of the HFD gut microbes into the ND-maintained (HFD-FMT) mice resulted in a significant decrease in spermatogenesis and sperm motility, whereas similar transplantation with the microbes from the ND-fed mice failed to do so. Analysis of the microbiota showed a profound increase in genus Bacteroides and Prevotella, both of which likely contributed to the metabolic endotoxaemia in the HFD-FMT mice. Interestingly, the gut microbes from clinical subjects revealed a strong negative correlation between the abundance of Bacteroides-Prevotella and sperm motility, and a positive correlation between blood endotoxin and Bacteroides abundance. Transplantation with HFD microbes also led to intestinal infiltration of T cells and macrophages as well as a significant increase of pro-inflammatory cytokines in the epididymis, suggesting that epididymal inflammation have likely contributed to the impairment of sperm motility. RNA-sequencing revealed significant reduction in the expression of those genes involved in gamete meiosis and testicular mitochondrial functions in the HFD-FMT mice.ConclusionWe revealed an intimate linkage between HFD-induced microbiota dysbiosis and defect in spermatogenesis with elevated endotoxin, dysregulation of testicular gene expression and localised epididymal inflammation as the potential causes.Trial registration numberNCT03634644. High-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can functionally influence spermatogenesis and sperm motility.OBJECTIVEHigh-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can functionally influence spermatogenesis and sperm motility.Faecal microbes derived from the HFD-fed or normal diet (ND)-fed male mice were transplanted to the mice maintained on ND. The gut microbes, sperm count and motility were analysed. Human faecal/semen/blood samples were collected to assess microbiota, sperm quality and endotoxin.DESIGNFaecal microbes derived from the HFD-fed or normal diet (ND)-fed male mice were transplanted to the mice maintained on ND. The gut microbes, sperm count and motility were analysed. Human faecal/semen/blood samples were collected to assess microbiota, sperm quality and endotoxin.Transplantation of the HFD gut microbes into the ND-maintained (HFD-FMT) mice resulted in a significant decrease in spermatogenesis and sperm motility, whereas similar transplantation with the microbes from the ND-fed mice failed to do so. Analysis of the microbiota showed a profound increase in genus Bacteroides and Prevotella, both of which likely contributed to the metabolic endotoxaemia in the HFD-FMT mice. Interestingly, the gut microbes from clinical subjects revealed a strong negative correlation between the abundance of Bacteroides-Prevotella and sperm motility, and a positive correlation between blood endotoxin and Bacteroides abundance. Transplantation with HFD microbes also led to intestinal infiltration of T cells and macrophages as well as a significant increase of pro-inflammatory cytokines in the epididymis, suggesting that epididymal inflammation have likely contributed to the impairment of sperm motility. RNA-sequencing revealed significant reduction in the expression of those genes involved in gamete meiosis and testicular mitochondrial functions in the HFD-FMT mice.RESULTSTransplantation of the HFD gut microbes into the ND-maintained (HFD-FMT) mice resulted in a significant decrease in spermatogenesis and sperm motility, whereas similar transplantation with the microbes from the ND-fed mice failed to do so. Analysis of the microbiota showed a profound increase in genus Bacteroides and Prevotella, both of which likely contributed to the metabolic endotoxaemia in the HFD-FMT mice. Interestingly, the gut microbes from clinical subjects revealed a strong negative correlation between the abundance of Bacteroides-Prevotella and sperm motility, and a positive correlation between blood endotoxin and Bacteroides abundance. Transplantation with HFD microbes also led to intestinal infiltration of T cells and macrophages as well as a significant increase of pro-inflammatory cytokines in the epididymis, suggesting that epididymal inflammation have likely contributed to the impairment of sperm motility. RNA-sequencing revealed significant reduction in the expression of those genes involved in gamete meiosis and testicular mitochondrial functions in the HFD-FMT mice.We revealed an intimate linkage between HFD-induced microbiota dysbiosis and defect in spermatogenesis with elevated endotoxin, dysregulation of testicular gene expression and localised epididymal inflammation as the potential causes.CONCLUSIONWe revealed an intimate linkage between HFD-induced microbiota dysbiosis and defect in spermatogenesis with elevated endotoxin, dysregulation of testicular gene expression and localised epididymal inflammation as the potential causes.NCT03634644.TRIAL REGISTRATION NUMBERNCT03634644.
Author	Zhang, Xin Peng, Li Li Zhang, Xue Di Li, Fang Hong Yan, Yun Jing Yao, Bing Ding, Ning Xiao, Geng Miao Jing, Jun Bi, Xin Yun Liu, Shan Shan Zhao, Allan Z Mu, Yun Ping Chen, Hao
AuthorAffiliation	6 The School of Biology and Biological Engineering , South China University of Technology , Guangzhou , Guangdong , China 2 Dizal Pharma , Shanghai , China 4 State Key Laboratory of Reproductive Medicine , Nanjing Medical University , Nanjing , Jiangsu , China 1 The School of Biomedical and Pharmaceutical Sciences , Guangdong University of Technology , Guangzhou , Guangdong , China 3 Jinling Hospital Department Reproductive Medical Center , Nanjing Medicine University , Nanjing , Jiangsu , China 5 Department of Laboratory , Women and Children 's Hospital of Qingdao , Qingdao , Shandong , China
AuthorAffiliation_xml	– name: 1 The School of Biomedical and Pharmaceutical Sciences , Guangdong University of Technology , Guangzhou , Guangdong , China – name: 6 The School of Biology and Biological Engineering , South China University of Technology , Guangzhou , Guangdong , China – name: 3 Jinling Hospital Department Reproductive Medical Center , Nanjing Medicine University , Nanjing , Jiangsu , China – name: 4 State Key Laboratory of Reproductive Medicine , Nanjing Medical University , Nanjing , Jiangsu , China – name: 2 Dizal Pharma , Shanghai , China – name: 5 Department of Laboratory , Women and Children 's Hospital of Qingdao , Qingdao , Shandong , China
Author_xml	– sequence: 1 givenname: Ning orcidid: 0000-0002-1826-1749 surname: Ding fullname: Ding, Ning organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 2 givenname: Xin surname: Zhang fullname: Zhang, Xin organization: Dizal Pharma, Shanghai, China – sequence: 3 givenname: Xue Di surname: Zhang fullname: Zhang, Xue Di organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 4 givenname: Jun surname: Jing fullname: Jing, Jun organization: State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China – sequence: 5 givenname: Shan Shan surname: Liu fullname: Liu, Shan Shan organization: Department of Laboratory, Women and Children 's Hospital of Qingdao, Qingdao, Shandong, China – sequence: 6 givenname: Yun Ping surname: Mu fullname: Mu, Yun Ping organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 7 givenname: Li Li orcidid: 0000-0001-9818-8301 surname: Peng fullname: Peng, Li Li organization: The School of Biology and Biological Engineering, South China University of Technology, Guangzhou, Guangdong, China – sequence: 8 givenname: Yun Jing surname: Yan fullname: Yan, Yun Jing organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 9 givenname: Geng Miao surname: Xiao fullname: Xiao, Geng Miao organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 10 givenname: Xin Yun surname: Bi fullname: Bi, Xin Yun organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 11 givenname: Hao surname: Chen fullname: Chen, Hao email: chenhao@gdut.edu.cn organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 12 givenname: Fang Hong surname: Li fullname: Li, Fang Hong email: fli@gdut.edu.cn organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China – sequence: 13 givenname: Bing surname: Yao fullname: Yao, Bing email: yaobing@nju.edu.cn organization: State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China – sequence: 14 givenname: Allan Z surname: Zhao fullname: Zhao, Allan Z email: azzhao@gdut.edu.cn organization: The School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, Guangdong, China
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31900292$$D View this record in MEDLINE/PubMed
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Snippet	ObjectiveHigh-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis... High-fat diet (HFD)-induced metabolic disorders can lead to impaired sperm production. We aim to investigate if HFD-induced gut microbiota dysbiosis can...
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SubjectTerms	Animals Antibodies Bacteroides Bacteroides - isolation & purification Chronic illnesses Correlation of Data Cytokines Cytokines - analysis Deoxyribonucleic acid Diabetes Diet Diet, High-Fat - adverse effects Digestive system DNA Dysbacteriosis Dysbiosis - etiology Dysbiosis - microbiology Endotoxemia - microbiology endotoxin Epididymis Epididymis - immunology Epididymis - pathology Feces - microbiology Gastric motility Gastrointestinal Microbiome - immunology Gastrointestinal tract Gene expression Glucose Gut Microbiota High fat diet Humans Infertility Inflammation intestinal microbiology Intestinal microflora Intestine Lymphocytes T Macrophages Macrophages - immunology Male Meiosis Metabolic disorders Mice Microbiota Microorganisms Mitochondria Motility Obesity Prevotella Prevotella - isolation & purification Ribonucleic acid RNA Sperm Sperm Motility - immunology Spermatogenesis Spermatogenesis - immunology T-Lymphocytes - immunology Testes Transplantation
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Title	Impairment of spermatogenesis and sperm motility by the high-fat diet-induced dysbiosis of gut microbes
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