Retinoic Acid Signaling Modulates Recipient Gut Barrier Integrity and Microbiota After Allogeneic Hematopoietic Stem Cell Transplantation in Mice
Graft-versus-host disease (GVHD) remains a major complication after allogeneic hematopoietic stem cell transplantation (HSCT). An impaired intestinal epithelial barrier is an important component of GVHD pathogenesis. However, contributing host factors that modulate mucosal barrier integrity during G...
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Published in | Frontiers in immunology Vol. 12; p. 749002 |
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Abstract | Graft-versus-host disease (GVHD) remains a major complication after allogeneic hematopoietic stem cell transplantation (HSCT). An impaired intestinal epithelial barrier is an important component of GVHD pathogenesis. However, contributing host factors that modulate mucosal barrier integrity during GVHD are poorly defined. We hypothesized that vitamin A and retinoic acid (RA) exert positive impacts on maintaining intestinal barrier function after HSCT, thus preventing or dampening GVHD severity. Unexpectedly, we found that exogenous RA increased intestinal permeability of recipient mice after allogeneic HSCT. Serum bacterial endotoxin levels were significantly higher in GVHD mice fed a vitamin A-high (VAH) diet compared to those fed a vitamin A-normal (VAN) diet, indicating a more compromised intestinal barrier function. Furthermore, VAH mice showed more severe lung GVHD with increased donor T cell infiltration in this tissue and died significantly faster than VAN recipients. 16S rRNA sequencing of fecal samples revealed significant differences in the diversity and composition of gut microbiota between VAN and VAH transplant recipients. Collectively, we show that retinoic acid signaling may negatively impact intestinal barrier function during GVHD. Mild vitamin A supplementation is associated with increased lung GVHD and more profound gut dysbiosis. Micronutrients such as vitamin A could modulate complications of allogeneic HSCT, which may be mediated by shaping gut microbiota. |
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AbstractList | Graft-versus-host disease (GVHD) remains a major complication after allogeneic hematopoietic stem cell transplantation (HSCT). An impaired intestinal epithelial barrier is an important component of GVHD pathogenesis. However, contributing host factors that modulate mucosal barrier integrity during GVHD are poorly defined. We hypothesized that vitamin A and retinoic acid (RA) exert positive impacts on maintaining intestinal barrier function after HSCT, thus preventing or dampening GVHD severity. Unexpectedly, we found that exogenous RA increased intestinal permeability of recipient mice after allogeneic HSCT. Serum bacterial endotoxin levels were significantly higher in GVHD mice fed a vitamin A-high (VAH) diet compared to those fed a vitamin A-normal (VAN) diet, indicating a more compromised intestinal barrier function. Furthermore, VAH mice showed more severe lung GVHD with increased donor T cell infiltration in this tissue and died significantly faster than VAN recipients. 16S rRNA sequencing of fecal samples revealed significant differences in the diversity and composition of gut microbiota between VAN and VAH transplant recipients. Collectively, we show that retinoic acid signaling may negatively impact intestinal barrier function during GVHD. Mild vitamin A supplementation is associated with increased lung GVHD and more profound gut dysbiosis. Micronutrients such as vitamin A could modulate complications of allogeneic HSCT, which may be mediated by shaping gut microbiota. |
Author | Atkinson, Samantha N Wang, Li-Shu Gunsolus, Ian L Pan, Pan Taylor, Brian Liu, Chen Zhou, Dian Chen, Xiao Zhu, Haojie Morse, Matthew Flejsierowicz, Philip |
AuthorAffiliation | 1 Division of Hematology & Oncology, Medical College of Wisconsin , Milwaukee, WI , United States 5 Department of Pathology, Yale University School of Medicine , New Haven, CT , United States 3 Center for Microbiome Research, Medical College of Wisconsin , Milwaukee, WI , United States 6 Department of Pathology, Medical College of Wisconsin , Milwaukee, WI , United States 2 Department of Medicine, Medical College of Wisconsin , Milwaukee, WI , United States 4 Department of Microbiology and Immunology, Medical College of Wisconsin , Milwaukee, WI , United States |
AuthorAffiliation_xml | – name: 6 Department of Pathology, Medical College of Wisconsin , Milwaukee, WI , United States – name: 1 Division of Hematology & Oncology, Medical College of Wisconsin , Milwaukee, WI , United States – name: 5 Department of Pathology, Yale University School of Medicine , New Haven, CT , United States – name: 3 Center for Microbiome Research, Medical College of Wisconsin , Milwaukee, WI , United States – name: 2 Department of Medicine, Medical College of Wisconsin , Milwaukee, WI , United States – name: 4 Department of Microbiology and Immunology, Medical College of Wisconsin , Milwaukee, WI , United States |
Author_xml | – sequence: 1 givenname: Pan surname: Pan fullname: Pan, Pan organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 2 givenname: Samantha N surname: Atkinson fullname: Atkinson, Samantha N organization: Department of Microbiology and Immunology, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 3 givenname: Brian surname: Taylor fullname: Taylor, Brian organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 4 givenname: Haojie surname: Zhu fullname: Zhu, Haojie organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 5 givenname: Dian surname: Zhou fullname: Zhou, Dian organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 6 givenname: Philip surname: Flejsierowicz fullname: Flejsierowicz, Philip organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 7 givenname: Li-Shu surname: Wang fullname: Wang, Li-Shu organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 8 givenname: Matthew surname: Morse fullname: Morse, Matthew organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 9 givenname: Chen surname: Liu fullname: Liu, Chen organization: Department of Pathology, Yale University School of Medicine, New Haven, CT, United States – sequence: 10 givenname: Ian L surname: Gunsolus fullname: Gunsolus, Ian L organization: Department of Pathology, Medical College of Wisconsin, Milwaukee, WI, United States – sequence: 11 givenname: Xiao surname: Chen fullname: Chen, Xiao organization: Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, United States |
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Copyright | Copyright © 2021 Pan, Atkinson, Taylor, Zhu, Zhou, Flejsierowicz, Wang, Morse, Liu, Gunsolus and Chen. Copyright © 2021 Pan, Atkinson, Taylor, Zhu, Zhou, Flejsierowicz, Wang, Morse, Liu, Gunsolus and Chen 2021 Pan, Atkinson, Taylor, Zhu, Zhou, Flejsierowicz, Wang, Morse, Liu, Gunsolus and Chen |
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Keywords | retinoic acid vitamin A intestinal barrier graft-versus-host disease gut microbiota |
Language | English |
License | Copyright © 2021 Pan, Atkinson, Taylor, Zhu, Zhou, Flejsierowicz, Wang, Morse, Liu, Gunsolus and Chen. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Xuefang Cao, University of Maryland, United States; Meng Lv, Peking University People’s Hospital, China This article was submitted to Alloimmunity and Transplantation, a section of the journal Frontiers in Immunology Edited by: Xue-Zhong Yu, Medical University of South Carolina, United States |
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SubjectTerms | Animals Caco-2 Cells Feces - microbiology Gastrointestinal Microbiome - drug effects Gastrointestinal Microbiome - genetics Graft vs Host Disease graft-versus-host disease gut microbiota Hematopoietic Stem Cell Transplantation Humans Immunology intestinal barrier Intestinal Mucosa - drug effects Intestinal Mucosa - metabolism Lung - drug effects Male Mice Mice, Inbred BALB C Mice, Inbred C57BL Permeability - drug effects retinoic acid RNA, Ribosomal, 16S Signal Transduction - drug effects Transplantation, Homologous vitamin A Vitamin A - pharmacology Vitamins - pharmacology |
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Title | Retinoic Acid Signaling Modulates Recipient Gut Barrier Integrity and Microbiota After Allogeneic Hematopoietic Stem Cell Transplantation in Mice |
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