Bacteroides ovatus alleviates dysbiotic microbiota-induced graft-versus-host disease
Acute lower gastrointestinal GVHD (aLGI-GVHD) is a serious complication of allogeneic hematopoietic stem cell transplantation. Although the intestinal microbiota is associated with the incidence of aLGI-GVHD, how the intestinal microbiota impacts treatment responses in aLGI-GVHD has not been thoroug...
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creator | Hayase, Eiko Hayase, Tomo Mukherjee, Akash Stinson, Stuart C. Jamal, Mohamed A. Ortega, Miriam R. Sanchez, Christopher A. Ahmed, Saira S. Karmouch, Jennifer L. Chang, Chia-Chi Flores, Ivonne I. McDaniel, Lauren K. Brown, Alexandria N. El-Himri, Rawan K. Chapa, Valerie A. Tan, Lin Tran, Bao Q. Xiao, Yao Fan, Christopher Pham, Dung Halsey, Taylor M. Jin, Yimei Tsai, Wen-Bin Prasad, Rishika Glover, Israel K. Enkhbayar, Altai Mohammed, Aqsa Schmiester, Maren King, Katherine Y. Britton, Robert A. Reddy, Pavan Wong, Matthew C. Ajami, Nadim J. Wargo, Jennifer A. Shelburne, Samuel Okhuysen, Pablo C. Liu, Chen Fowler, Stephanie W. Conner, Margaret E. Katsamakis, Zoe Smith, Natalie Burgos da Silva, Marina Ponce, Doris M. Peled, Jonathan U. van den Brink, Marcel R.M. Peterson, Christine B. Rondon, Gabriela Molldrem, Jeffrey J. Champlin, Richard E. Shpall, Elizabeth J. Lorenzi, Philip L. Mehta, Rohtesh S. Martens, Eric C. Alousi, Amin M. Jenq, Robert R. |
description | Acute lower gastrointestinal GVHD (aLGI-GVHD) is a serious complication of allogeneic hematopoietic stem cell transplantation. Although the intestinal microbiota is associated with the incidence of aLGI-GVHD, how the intestinal microbiota impacts treatment responses in aLGI-GVHD has not been thoroughly studied. In a cohort of patients with aLGI-GVHD (n = 37), we found that non-response to standard therapy with corticosteroids was associated with prior treatment with carbapenem antibiotics and a disrupted fecal microbiome characterized by reduced abundances of Bacteroides ovatus. In a murine GVHD model aggravated by carbapenem antibiotics, introducing B. ovatus reduced GVHD severity and improved survival. These beneficial effects of Bacteroides ovatus were linked to its ability to metabolize dietary polysaccharides into monosaccharides, which suppressed the mucus-degrading capabilities of colonic mucus degraders such as Bacteroides thetaiotaomicron and Akkermansia muciniphila, thus reducing GVHD-related mortality. Collectively, these findings reveal the importance of microbiota in aLGI-GVHD and therapeutic potential of B. ovatus.
[Display omitted]
•Clinical steroid-refractory GVHD is associated with reduced Bacteroides ovatus•Introduction of B. ovatus after meropenem reduces experimental GVHD-related mortality•The beneficial effects of B. ovatus are linked to its ability to produce xylose•B. ovatus suppresses the mucus-degrading capabilities of colonic mucus degraders
Hayase et al. discover that Bacteroides ovatus reduces the severity of graft-versus-host disease (GVHD), a complication of hematopoietic cell transplantation, by suppressing mucus-degrading gut microbes. These beneficial effects of B. ovatus are linked to the metabolism of dietary polysaccharides into monosaccharides and highlight the therapeutic potential of B. ovatus. |
doi_str_mv | 10.1016/j.chom.2024.08.004 |
format | Article |
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[Display omitted]
•Clinical steroid-refractory GVHD is associated with reduced Bacteroides ovatus•Introduction of B. ovatus after meropenem reduces experimental GVHD-related mortality•The beneficial effects of B. ovatus are linked to its ability to produce xylose•B. ovatus suppresses the mucus-degrading capabilities of colonic mucus degraders
Hayase et al. discover that Bacteroides ovatus reduces the severity of graft-versus-host disease (GVHD), a complication of hematopoietic cell transplantation, by suppressing mucus-degrading gut microbes. These beneficial effects of B. ovatus are linked to the metabolism of dietary polysaccharides into monosaccharides and highlight the therapeutic potential of B. ovatus.</description><identifier>ISSN: 1931-3128</identifier><identifier>ISSN: 1934-6069</identifier><identifier>EISSN: 1934-6069</identifier><identifier>DOI: 10.1016/j.chom.2024.08.004</identifier><identifier>PMID: 39214085</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adult ; Akkermansia ; Akkermansia muciniphila ; allogeneic hematopoietic stem cell transplantation ; Animals ; Bacteroides - drug effects ; Bacteroides ovatus ; Bacteroides thetaiotaomicron ; Bacteroides thetaiotaomicron - drug effects ; Disease Models, Animal ; Dysbiosis - microbiology ; Feces - microbiology ; Female ; Gastrointestinal Microbiome - drug effects ; Graft vs Host Disease - microbiology ; graft-versus-host disease ; Hematopoietic Stem Cell Transplantation ; Humans ; intestinal microbiome ; Male ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Middle Aged ; mucus layer ; polysaccharide utilization loci ; polysaccharides ; xylose</subject><ispartof>Cell host & microbe, 2024-09, Vol.32 (9), p.1621-1636.e6</ispartof><rights>2024 Elsevier Inc.</rights><rights>Copyright © 2024 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c237t-1357ee3350b505f966838ffb4c1d1098d81bbd6f1d4599aad96b385291942af13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.chom.2024.08.004$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>315,781,785,3551,27929,27930,46000</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39214085$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hayase, Eiko</creatorcontrib><creatorcontrib>Hayase, Tomo</creatorcontrib><creatorcontrib>Mukherjee, Akash</creatorcontrib><creatorcontrib>Stinson, Stuart C.</creatorcontrib><creatorcontrib>Jamal, Mohamed A.</creatorcontrib><creatorcontrib>Ortega, Miriam R.</creatorcontrib><creatorcontrib>Sanchez, Christopher A.</creatorcontrib><creatorcontrib>Ahmed, Saira S.</creatorcontrib><creatorcontrib>Karmouch, Jennifer L.</creatorcontrib><creatorcontrib>Chang, Chia-Chi</creatorcontrib><creatorcontrib>Flores, Ivonne I.</creatorcontrib><creatorcontrib>McDaniel, Lauren K.</creatorcontrib><creatorcontrib>Brown, Alexandria N.</creatorcontrib><creatorcontrib>El-Himri, Rawan K.</creatorcontrib><creatorcontrib>Chapa, Valerie A.</creatorcontrib><creatorcontrib>Tan, Lin</creatorcontrib><creatorcontrib>Tran, Bao Q.</creatorcontrib><creatorcontrib>Xiao, Yao</creatorcontrib><creatorcontrib>Fan, Christopher</creatorcontrib><creatorcontrib>Pham, Dung</creatorcontrib><creatorcontrib>Halsey, Taylor M.</creatorcontrib><creatorcontrib>Jin, Yimei</creatorcontrib><creatorcontrib>Tsai, Wen-Bin</creatorcontrib><creatorcontrib>Prasad, Rishika</creatorcontrib><creatorcontrib>Glover, Israel K.</creatorcontrib><creatorcontrib>Enkhbayar, Altai</creatorcontrib><creatorcontrib>Mohammed, Aqsa</creatorcontrib><creatorcontrib>Schmiester, Maren</creatorcontrib><creatorcontrib>King, Katherine Y.</creatorcontrib><creatorcontrib>Britton, Robert A.</creatorcontrib><creatorcontrib>Reddy, Pavan</creatorcontrib><creatorcontrib>Wong, Matthew C.</creatorcontrib><creatorcontrib>Ajami, Nadim J.</creatorcontrib><creatorcontrib>Wargo, Jennifer A.</creatorcontrib><creatorcontrib>Shelburne, Samuel</creatorcontrib><creatorcontrib>Okhuysen, Pablo C.</creatorcontrib><creatorcontrib>Liu, Chen</creatorcontrib><creatorcontrib>Fowler, Stephanie W.</creatorcontrib><creatorcontrib>Conner, Margaret E.</creatorcontrib><creatorcontrib>Katsamakis, Zoe</creatorcontrib><creatorcontrib>Smith, Natalie</creatorcontrib><creatorcontrib>Burgos da Silva, Marina</creatorcontrib><creatorcontrib>Ponce, Doris M.</creatorcontrib><creatorcontrib>Peled, Jonathan U.</creatorcontrib><creatorcontrib>van den Brink, Marcel R.M.</creatorcontrib><creatorcontrib>Peterson, Christine B.</creatorcontrib><creatorcontrib>Rondon, Gabriela</creatorcontrib><creatorcontrib>Molldrem, Jeffrey J.</creatorcontrib><creatorcontrib>Champlin, Richard E.</creatorcontrib><creatorcontrib>Shpall, Elizabeth J.</creatorcontrib><creatorcontrib>Lorenzi, Philip L.</creatorcontrib><creatorcontrib>Mehta, Rohtesh S.</creatorcontrib><creatorcontrib>Martens, Eric C.</creatorcontrib><creatorcontrib>Alousi, Amin M.</creatorcontrib><creatorcontrib>Jenq, Robert R.</creatorcontrib><title>Bacteroides ovatus alleviates dysbiotic microbiota-induced graft-versus-host disease</title><title>Cell host & microbe</title><addtitle>Cell Host Microbe</addtitle><description>Acute lower gastrointestinal GVHD (aLGI-GVHD) is a serious complication of allogeneic hematopoietic stem cell transplantation. Although the intestinal microbiota is associated with the incidence of aLGI-GVHD, how the intestinal microbiota impacts treatment responses in aLGI-GVHD has not been thoroughly studied. In a cohort of patients with aLGI-GVHD (n = 37), we found that non-response to standard therapy with corticosteroids was associated with prior treatment with carbapenem antibiotics and a disrupted fecal microbiome characterized by reduced abundances of Bacteroides ovatus. In a murine GVHD model aggravated by carbapenem antibiotics, introducing B. ovatus reduced GVHD severity and improved survival. These beneficial effects of Bacteroides ovatus were linked to its ability to metabolize dietary polysaccharides into monosaccharides, which suppressed the mucus-degrading capabilities of colonic mucus degraders such as Bacteroides thetaiotaomicron and Akkermansia muciniphila, thus reducing GVHD-related mortality. Collectively, these findings reveal the importance of microbiota in aLGI-GVHD and therapeutic potential of B. ovatus.
[Display omitted]
•Clinical steroid-refractory GVHD is associated with reduced Bacteroides ovatus•Introduction of B. ovatus after meropenem reduces experimental GVHD-related mortality•The beneficial effects of B. ovatus are linked to its ability to produce xylose•B. ovatus suppresses the mucus-degrading capabilities of colonic mucus degraders
Hayase et al. discover that Bacteroides ovatus reduces the severity of graft-versus-host disease (GVHD), a complication of hematopoietic cell transplantation, by suppressing mucus-degrading gut microbes. These beneficial effects of B. ovatus are linked to the metabolism of dietary polysaccharides into monosaccharides and highlight the therapeutic potential of B. ovatus.</description><subject>Adult</subject><subject>Akkermansia</subject><subject>Akkermansia muciniphila</subject><subject>allogeneic hematopoietic stem cell transplantation</subject><subject>Animals</subject><subject>Bacteroides - drug effects</subject><subject>Bacteroides ovatus</subject><subject>Bacteroides thetaiotaomicron</subject><subject>Bacteroides thetaiotaomicron - drug effects</subject><subject>Disease Models, Animal</subject><subject>Dysbiosis - microbiology</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Gastrointestinal Microbiome - drug effects</subject><subject>Graft vs Host Disease - microbiology</subject><subject>graft-versus-host disease</subject><subject>Hematopoietic Stem Cell Transplantation</subject><subject>Humans</subject><subject>intestinal microbiome</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Middle Aged</subject><subject>mucus layer</subject><subject>polysaccharide utilization 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Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20240911</creationdate><title>Bacteroides ovatus alleviates dysbiotic microbiota-induced graft-versus-host disease</title><author>Hayase, Eiko ; Hayase, Tomo ; Mukherjee, Akash ; Stinson, Stuart C. ; Jamal, Mohamed A. ; Ortega, Miriam R. ; Sanchez, Christopher A. ; Ahmed, Saira S. ; Karmouch, Jennifer L. ; Chang, Chia-Chi ; Flores, Ivonne I. ; McDaniel, Lauren K. ; Brown, Alexandria N. ; El-Himri, Rawan K. ; Chapa, Valerie A. ; Tan, Lin ; Tran, Bao Q. ; Xiao, Yao ; Fan, Christopher ; Pham, Dung ; Halsey, Taylor M. ; Jin, Yimei ; Tsai, Wen-Bin ; Prasad, Rishika ; Glover, Israel K. ; Enkhbayar, Altai ; Mohammed, Aqsa ; Schmiester, Maren ; King, Katherine Y. ; Britton, Robert A. ; Reddy, Pavan ; Wong, Matthew C. ; Ajami, Nadim J. ; Wargo, Jennifer A. ; Shelburne, Samuel ; Okhuysen, 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K.</creatorcontrib><creatorcontrib>Enkhbayar, Altai</creatorcontrib><creatorcontrib>Mohammed, Aqsa</creatorcontrib><creatorcontrib>Schmiester, Maren</creatorcontrib><creatorcontrib>King, Katherine Y.</creatorcontrib><creatorcontrib>Britton, Robert A.</creatorcontrib><creatorcontrib>Reddy, Pavan</creatorcontrib><creatorcontrib>Wong, Matthew C.</creatorcontrib><creatorcontrib>Ajami, Nadim J.</creatorcontrib><creatorcontrib>Wargo, Jennifer A.</creatorcontrib><creatorcontrib>Shelburne, Samuel</creatorcontrib><creatorcontrib>Okhuysen, Pablo C.</creatorcontrib><creatorcontrib>Liu, Chen</creatorcontrib><creatorcontrib>Fowler, Stephanie W.</creatorcontrib><creatorcontrib>Conner, Margaret E.</creatorcontrib><creatorcontrib>Katsamakis, Zoe</creatorcontrib><creatorcontrib>Smith, Natalie</creatorcontrib><creatorcontrib>Burgos da Silva, Marina</creatorcontrib><creatorcontrib>Ponce, Doris M.</creatorcontrib><creatorcontrib>Peled, Jonathan U.</creatorcontrib><creatorcontrib>van den Brink, Marcel R.M.</creatorcontrib><creatorcontrib>Peterson, Christine B.</creatorcontrib><creatorcontrib>Rondon, Gabriela</creatorcontrib><creatorcontrib>Molldrem, Jeffrey J.</creatorcontrib><creatorcontrib>Champlin, Richard E.</creatorcontrib><creatorcontrib>Shpall, Elizabeth J.</creatorcontrib><creatorcontrib>Lorenzi, Philip L.</creatorcontrib><creatorcontrib>Mehta, Rohtesh S.</creatorcontrib><creatorcontrib>Martens, Eric C.</creatorcontrib><creatorcontrib>Alousi, Amin M.</creatorcontrib><creatorcontrib>Jenq, Robert R.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Cell host & microbe</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hayase, Eiko</au><au>Hayase, Tomo</au><au>Mukherjee, Akash</au><au>Stinson, Stuart C.</au><au>Jamal, Mohamed A.</au><au>Ortega, Miriam R.</au><au>Sanchez, Christopher A.</au><au>Ahmed, Saira S.</au><au>Karmouch, Jennifer L.</au><au>Chang, Chia-Chi</au><au>Flores, Ivonne I.</au><au>McDaniel, Lauren K.</au><au>Brown, Alexandria N.</au><au>El-Himri, Rawan K.</au><au>Chapa, Valerie A.</au><au>Tan, Lin</au><au>Tran, Bao Q.</au><au>Xiao, Yao</au><au>Fan, Christopher</au><au>Pham, Dung</au><au>Halsey, Taylor M.</au><au>Jin, Yimei</au><au>Tsai, Wen-Bin</au><au>Prasad, Rishika</au><au>Glover, Israel K.</au><au>Enkhbayar, Altai</au><au>Mohammed, Aqsa</au><au>Schmiester, Maren</au><au>King, Katherine Y.</au><au>Britton, Robert A.</au><au>Reddy, Pavan</au><au>Wong, Matthew C.</au><au>Ajami, Nadim J.</au><au>Wargo, Jennifer A.</au><au>Shelburne, Samuel</au><au>Okhuysen, Pablo C.</au><au>Liu, Chen</au><au>Fowler, Stephanie W.</au><au>Conner, Margaret E.</au><au>Katsamakis, Zoe</au><au>Smith, Natalie</au><au>Burgos da Silva, Marina</au><au>Ponce, Doris M.</au><au>Peled, Jonathan U.</au><au>van den Brink, Marcel R.M.</au><au>Peterson, Christine B.</au><au>Rondon, Gabriela</au><au>Molldrem, Jeffrey J.</au><au>Champlin, Richard E.</au><au>Shpall, Elizabeth J.</au><au>Lorenzi, Philip L.</au><au>Mehta, Rohtesh S.</au><au>Martens, Eric C.</au><au>Alousi, Amin M.</au><au>Jenq, Robert R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bacteroides ovatus alleviates dysbiotic microbiota-induced graft-versus-host disease</atitle><jtitle>Cell host & microbe</jtitle><addtitle>Cell Host Microbe</addtitle><date>2024-09-11</date><risdate>2024</risdate><volume>32</volume><issue>9</issue><spage>1621</spage><epage>1636.e6</epage><pages>1621-1636.e6</pages><issn>1931-3128</issn><issn>1934-6069</issn><eissn>1934-6069</eissn><abstract>Acute lower gastrointestinal GVHD (aLGI-GVHD) is a serious complication of allogeneic hematopoietic stem cell transplantation. Although the intestinal microbiota is associated with the incidence of aLGI-GVHD, how the intestinal microbiota impacts treatment responses in aLGI-GVHD has not been thoroughly studied. In a cohort of patients with aLGI-GVHD (n = 37), we found that non-response to standard therapy with corticosteroids was associated with prior treatment with carbapenem antibiotics and a disrupted fecal microbiome characterized by reduced abundances of Bacteroides ovatus. In a murine GVHD model aggravated by carbapenem antibiotics, introducing B. ovatus reduced GVHD severity and improved survival. These beneficial effects of Bacteroides ovatus were linked to its ability to metabolize dietary polysaccharides into monosaccharides, which suppressed the mucus-degrading capabilities of colonic mucus degraders such as Bacteroides thetaiotaomicron and Akkermansia muciniphila, thus reducing GVHD-related mortality. Collectively, these findings reveal the importance of microbiota in aLGI-GVHD and therapeutic potential of B. ovatus.
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•Clinical steroid-refractory GVHD is associated with reduced Bacteroides ovatus•Introduction of B. ovatus after meropenem reduces experimental GVHD-related mortality•The beneficial effects of B. ovatus are linked to its ability to produce xylose•B. ovatus suppresses the mucus-degrading capabilities of colonic mucus degraders
Hayase et al. discover that Bacteroides ovatus reduces the severity of graft-versus-host disease (GVHD), a complication of hematopoietic cell transplantation, by suppressing mucus-degrading gut microbes. These beneficial effects of B. ovatus are linked to the metabolism of dietary polysaccharides into monosaccharides and highlight the therapeutic potential of B. ovatus.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>39214085</pmid><doi>10.1016/j.chom.2024.08.004</doi></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1931-3128 |
ispartof | Cell host & microbe, 2024-09, Vol.32 (9), p.1621-1636.e6 |
issn | 1931-3128 1934-6069 1934-6069 |
language | eng |
recordid | cdi_proquest_miscellaneous_3099805608 |
source | MEDLINE; Access via ScienceDirect (Elsevier) |
subjects | Adult Akkermansia Akkermansia muciniphila allogeneic hematopoietic stem cell transplantation Animals Bacteroides - drug effects Bacteroides ovatus Bacteroides thetaiotaomicron Bacteroides thetaiotaomicron - drug effects Disease Models, Animal Dysbiosis - microbiology Feces - microbiology Female Gastrointestinal Microbiome - drug effects Graft vs Host Disease - microbiology graft-versus-host disease Hematopoietic Stem Cell Transplantation Humans intestinal microbiome Male Mice Mice, Inbred BALB C Mice, Inbred C57BL Middle Aged mucus layer polysaccharide utilization loci polysaccharides xylose |
title | Bacteroides ovatus alleviates dysbiotic microbiota-induced graft-versus-host disease |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-12T14%3A41%3A44IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Bacteroides%20ovatus%20alleviates%20dysbiotic%20microbiota-induced%20graft-versus-host%20disease&rft.jtitle=Cell%20host%20&%20microbe&rft.au=Hayase,%20Eiko&rft.date=2024-09-11&rft.volume=32&rft.issue=9&rft.spage=1621&rft.epage=1636.e6&rft.pages=1621-1636.e6&rft.issn=1931-3128&rft.eissn=1934-6069&rft_id=info:doi/10.1016/j.chom.2024.08.004&rft_dat=%3Cproquest_cross%3E3099805608%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3099805608&rft_id=info:pmid/39214085&rft_els_id=S1931312824002919&rfr_iscdi=true |