D-amino Acids Ameliorate Experimental Colitis and Cholangitis by Inhibiting Growth of Proteobacteria: Potential Therapeutic Role in Inflammatory Bowel Disease
D-amino acids, the chiral counterparts of protein L-amino acids, were primarily produced and utilized by microbes, including those in the human gut. However, little was known about how orally administered or microbe-derived D-amino acids affected the gut microbial community or gut disease progressio...
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Published in | Cellular and molecular gastroenterology and hepatology Vol. 16; no. 6; pp. 1011 - 1031 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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Language | English |
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01.01.2023
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Abstract | D-amino acids, the chiral counterparts of protein L-amino acids, were primarily produced and utilized by microbes, including those in the human gut. However, little was known about how orally administered or microbe-derived D-amino acids affected the gut microbial community or gut disease progression.
The ratio of D- to L-amino acids was analyzed in feces and blood from patients with ulcerative colitis (UC) and healthy controls. Also, composition of microbe was analyzed from patients with UC. Mice were treated with D-amino acid in dextran sulfate sodium colitis model and liver cholangitis model.
The ratio of D- to L-amino acids was lower in the feces of patients with UC than that of healthy controls. Supplementation of D-amino acids ameliorated UC-related experimental colitis and liver cholangitis by inhibiting growth of Proteobacteria. Addition of D-alanine, a major building block for bacterial cell wall formation, to culture medium inhibited expression of the ftsZ gene required for cell fission in the Proteobacteria Escherichia coli and Klebsiella pneumoniae, thereby inhibiting growth. Overexpression of ftsZ restored growth of E. coli even when D-alanine was present. We found that D-alanine not only inhibited invasion of pathological K. pneumoniae into the host via pore formation in intestinal epithelial cells but also inhibited growth of E. coli and generation of antibiotic-resistant strains.
D-amino acids might have potential for use in novel therapeutic approaches targeting Proteobacteria-associated dysbiosis and antibiotic-resistant bacterial diseases by means of their effects on the intestinal microbiota community.
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AbstractList | D-amino acids, the chiral counterparts of protein L-amino acids, were primarily produced and utilized by microbes, including those in the human gut. However, little was known about how orally administered or microbe-derived D-amino acids affected the gut microbial community or gut disease progression.
The ratio of D- to L-amino acids was analyzed in feces and blood from patients with ulcerative colitis (UC) and healthy controls. Also, composition of microbe was analyzed from patients with UC. Mice were treated with D-amino acid in dextran sulfate sodium colitis model and liver cholangitis model.
The ratio of D- to L-amino acids was lower in the feces of patients with UC than that of healthy controls. Supplementation of D-amino acids ameliorated UC-related experimental colitis and liver cholangitis by inhibiting growth of Proteobacteria. Addition of D-alanine, a major building block for bacterial cell wall formation, to culture medium inhibited expression of the ftsZ gene required for cell fission in the Proteobacteria Escherichia coli and Klebsiella pneumoniae, thereby inhibiting growth. Overexpression of ftsZ restored growth of E. coli even when D-alanine was present. We found that D-alanine not only inhibited invasion of pathological K. pneumoniae into the host via pore formation in intestinal epithelial cells but also inhibited growth of E. coli and generation of antibiotic-resistant strains.
D-amino acids might have potential for use in novel therapeutic approaches targeting Proteobacteria-associated dysbiosis and antibiotic-resistant bacterial diseases by means of their effects on the intestinal microbiota community. D-amino acids, the chiral counterparts of protein L-amino acids, were primarily produced and utilized by microbes, including those in the human gut. However, little was known about how orally administered or microbe-derived D-amino acids affected the gut microbial community or gut disease progression. The ratio of D- to L-amino acids was analyzed in feces and blood from patients with ulcerative colitis (UC) and healthy controls. Also, composition of microbe was analyzed from patients with UC. Mice were treated with D-amino acid in dextran sulfate sodium colitis model and liver cholangitis model. The ratio of D- to L-amino acids was lower in the feces of patients with UC than that of healthy controls. Supplementation of D-amino acids ameliorated UC-related experimental colitis and liver cholangitis by inhibiting growth of Proteobacteria. Addition of D-alanine, a major building block for bacterial cell wall formation, to culture medium inhibited expression of the ftsZ gene required for cell fission in the Proteobacteria Escherichia coli and Klebsiella pneumoniae, thereby inhibiting growth. Overexpression of ftsZ restored growth of E. coli even when D-alanine was present. We found that D-alanine not only inhibited invasion of pathological K. pneumoniae into the host via pore formation in intestinal epithelial cells but also inhibited growth of E. coli and generation of antibiotic-resistant strains. D-amino acids might have potential for use in novel therapeutic approaches targeting Proteobacteria-associated dysbiosis and antibiotic-resistant bacterial diseases by means of their effects on the intestinal microbiota community. [Display omitted] BACKGROUND & AIMSD-amino acids, the chiral counterparts of protein L-amino acids, were primarily produced and utilized by microbes, including those in the human gut. However, little was known about how orally administered or microbe-derived D-amino acids affected the gut microbial community or gut disease progression.METHODSThe ratio of D- to L-amino acids was analyzed in feces and blood from patients with ulcerative colitis (UC) and healthy controls. Also, composition of microbe was analyzed from patients with UC. Mice were treated with D-amino acid in dextran sulfate sodium colitis model and liver cholangitis model.RESULTSThe ratio of D- to L-amino acids was lower in the feces of patients with UC than that of healthy controls. Supplementation of D-amino acids ameliorated UC-related experimental colitis and liver cholangitis by inhibiting growth of Proteobacteria. Addition of D-alanine, a major building block for bacterial cell wall formation, to culture medium inhibited expression of the ftsZ gene required for cell fission in the Proteobacteria Escherichia coli and Klebsiella pneumoniae, thereby inhibiting growth. Overexpression of ftsZ restored growth of E. coli even when D-alanine was present. We found that D-alanine not only inhibited invasion of pathological K. pneumoniae into the host via pore formation in intestinal epithelial cells but also inhibited growth of E. coli and generation of antibiotic-resistant strains.CONCLUSIONSD-amino acids might have potential for use in novel therapeutic approaches targeting Proteobacteria-associated dysbiosis and antibiotic-resistant bacterial diseases by means of their effects on the intestinal microbiota community. |
Author | Mikami, Yohei Umeda, Satoko Miyamoto, Kentaro Kanai, Takanori Shiomi, Daisuke Aoto, Yoshimasa Moritoki, Nobuko Teratani, Toshiaki Sasaki, Nobuo Suzuki, Toshihiko Amafuji, Kimiko Sujino, Tomohisa Takabayashi, Kaoru Mita, Masashi Sato, Toshiro Sasabe, Jumpei Hayashi, Naoki Hosoe, Naoki Atarashi, Koji Shibata, Shinsuke Nakamoto, Nobuhiro Tanemoto, Shun Ogata, Haruhiko Yoshimatsu, Yusuke Adachi, Keika Nishiyama, Keita Ashida, Hiroshi Ono, Keiko Harada, Yosuke |
Author_xml | – sequence: 1 givenname: Satoko surname: Umeda fullname: Umeda, Satoko organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 2 givenname: Tomohisa orcidid: 0000-0003-0699-6577 surname: Sujino fullname: Sujino, Tomohisa email: tsujino1224@keio.jp organization: Center for Diagnostic and Therapeutic Endoscopy, Keio University School of Medicine, Tokyo, Japan – sequence: 3 givenname: Kentaro surname: Miyamoto fullname: Miyamoto, Kentaro organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 4 givenname: Yusuke surname: Yoshimatsu fullname: Yoshimatsu, Yusuke organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 5 givenname: Yosuke surname: Harada fullname: Harada, Yosuke organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 6 givenname: Keita surname: Nishiyama fullname: Nishiyama, Keita organization: Department of Microbiology and Immunology, Keio University School of Medicine, Tokyo, Japan – sequence: 7 givenname: Yoshimasa surname: Aoto fullname: Aoto, Yoshimasa organization: JSR-Keio University Medical and Chemical Innovation Center (JKiC), JSR Corp, Tokyo, Japan – sequence: 8 givenname: Keika surname: Adachi fullname: Adachi, Keika organization: JSR-Keio University Medical and Chemical Innovation Center (JKiC), JSR Corp, Tokyo, Japan – sequence: 9 givenname: Naoki surname: Hayashi fullname: Hayashi, Naoki organization: JSR-Keio University Medical and Chemical Innovation Center (JKiC), JSR Corp, Tokyo, Japan – sequence: 10 givenname: Kimiko surname: Amafuji fullname: Amafuji, Kimiko organization: JSR-Keio University Medical and Chemical Innovation Center (JKiC), JSR Corp, Tokyo, Japan – sequence: 11 givenname: Nobuko surname: Moritoki fullname: Moritoki, Nobuko organization: Electron Microscope Laboratory, Keio University School of Medicine, Tokyo, Japan – sequence: 12 givenname: Shinsuke surname: Shibata fullname: Shibata, Shinsuke organization: Electron Microscope Laboratory, Keio University School of Medicine, Tokyo, Japan – sequence: 13 givenname: Nobuo surname: Sasaki fullname: Sasaki, Nobuo organization: Institute of Molecular and Cellular Regulation, Gunma University, Maebashi City, Japan – sequence: 14 givenname: Masashi surname: Mita fullname: Mita, Masashi organization: KAGAMI Inc, Osaka, Japan – sequence: 15 givenname: Shun surname: Tanemoto fullname: Tanemoto, Shun organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 16 givenname: Keiko surname: Ono fullname: Ono, Keiko organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 17 givenname: Yohei surname: Mikami fullname: Mikami, Yohei organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 18 givenname: Jumpei surname: Sasabe fullname: Sasabe, Jumpei organization: Department of Pharmacology, School of Medicine, Keio University, Tokyo, Japan – sequence: 19 givenname: Kaoru surname: Takabayashi fullname: Takabayashi, Kaoru organization: Center for Diagnostic and Therapeutic Endoscopy, Keio University School of Medicine, Tokyo, Japan – sequence: 20 givenname: Naoki surname: Hosoe fullname: Hosoe, Naoki organization: Center for Diagnostic and Therapeutic Endoscopy, Keio University School of Medicine, Tokyo, Japan – sequence: 21 givenname: Toshihiko surname: Suzuki fullname: Suzuki, Toshihiko organization: Department of Bacterial Infection and Host Response, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University (TMDU), Tokyo, Japan – sequence: 22 givenname: Toshiro surname: Sato fullname: Sato, Toshiro organization: Department of Organoid Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 23 givenname: Koji surname: Atarashi fullname: Atarashi, Koji organization: Department of Microbiology and Immunology, Keio University School of Medicine, Tokyo, Japan – sequence: 24 givenname: Toshiaki surname: Teratani fullname: Teratani, Toshiaki organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 25 givenname: Haruhiko surname: Ogata fullname: Ogata, Haruhiko organization: Center for Diagnostic and Therapeutic Endoscopy, Keio University School of Medicine, Tokyo, Japan – sequence: 26 givenname: Nobuhiro surname: Nakamoto fullname: Nakamoto, Nobuhiro organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan – sequence: 27 givenname: Daisuke surname: Shiomi fullname: Shiomi, Daisuke organization: Department of Life Science, College of Science, Rikkyo University, Tokyo, Japan – sequence: 28 givenname: Hiroshi surname: Ashida fullname: Ashida, Hiroshi organization: Department of Bacterial Infection and Host Response, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University (TMDU), Tokyo, Japan – sequence: 29 givenname: Takanori surname: Kanai fullname: Kanai, Takanori email: takagast@keio.jp organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan |
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Keywords | D-Amino Acid IBD ▪ Liver Cholangitis Microbiome K. pneumoniae ftsZ Ulcerative Colitis E.coli Colitis Inflammatory Bowel Disease Antibiotic-resistant Bacteria |
Language | English |
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Snippet | D-amino acids, the chiral counterparts of protein L-amino acids, were primarily produced and utilized by microbes, including those in the human gut. However,... BACKGROUND & AIMSD-amino acids, the chiral counterparts of protein L-amino acids, were primarily produced and utilized by microbes, including those in the... |
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SubjectTerms | Alanine Amino Acids Animals Anti-Bacterial Agents - pharmacology Anti-Bacterial Agents - therapeutic use Cholangitis - drug therapy Colitis - chemically induced Colitis - drug therapy Colitis, Ulcerative - chemically induced Colitis, Ulcerative - drug therapy D-Amino Acid Escherichia coli Humans IBD Inflammatory Bowel Diseases - drug therapy Liver Cholangitis Mice Microbiome Original Research Proteobacteria |
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Title | D-amino Acids Ameliorate Experimental Colitis and Cholangitis by Inhibiting Growth of Proteobacteria: Potential Therapeutic Role in Inflammatory Bowel Disease |
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