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      Research advances on short-chain fatty acids in gastrointestinal acute graft- versus-host disease

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          Abstract

          Gastrointestinal acute graft- versus-host disease (GI-aGVHD) is a severe early complication following allogeneic hematopoietic stem cell transplantation (allo-HSCT). It has been shown that the intestinal microbiota plays a critical role in this process. As metabolites of the intestinal microbiota, short-chain fatty acids (SCFAs) are vital for maintaining the host-microbiota symbiotic equilibrium. This article provides an overview of the protective effect of SCFAs in the gastrointestinal tract, emphasizes their association with GI-aGVHD, and explores relevant research progress in prevention and treatment research.

          Plain language summary

          Research advances on short-chain fatty acids in gastrointestinal acute graft-versus-host disease

          Gastrointestinal acute graft-versus-host disease (GI-aGVHD) is a severe early complication following allogeneic hematopoietic stem cell transplantation (allo-HSCT). It has been shown that the intestinal microbiota plays a critical role in this process. As metabolites of the intestinal microbiota, short-chain fatty acids (SCFAs) are vital for maintaining the host-microbiota symbiotic equilibrium. This article provides an overview of the protective effect of SCFAs in the gastrointestinal tract, emphasizes their association with GI-aGVHD and explores relevant research progress in prevention and treatment research.

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          Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic.

          Colin Hill, Francisco Guarner, Gregor Reid … (2014)
          An expert panel was convened in October 2013 by the International Scientific Association for Probiotics and Prebiotics (ISAPP) to discuss the field of probiotics. It is now 13 years since the definition of probiotics and 12 years after guidelines were published for regulators, scientists and industry by the Food and Agriculture Organization of the United Nations and the WHO (FAO/WHO). The FAO/WHO definition of a probiotic--"live microorganisms which when administered in adequate amounts confer a health benefit on the host"--was reinforced as relevant and sufficiently accommodating for current and anticipated applications. However, inconsistencies between the FAO/WHO Expert Consultation Report and the FAO/WHO Guidelines were clarified to take into account advances in science and applications. A more precise use of the term 'probiotic' will be useful to guide clinicians and consumers in differentiating the diverse products on the market. This document represents the conclusions of the ISAPP consensus meeting on the appropriate use and scope of the term probiotic.
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            The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.

            Patrick M. Smith, Michael R. Howitt, Nicolai Panikov … (2013)
            Regulatory T cells (Tregs) that express the transcription factor Foxp3 are critical for regulating intestinal inflammation. Candidate microbe approaches have identified bacterial species and strain-specific molecules that can affect intestinal immune responses, including species that modulate Treg responses. Because neither all humans nor mice harbor the same bacterial strains, we posited that more prevalent factors exist that regulate the number and function of colonic Tregs. We determined that short-chain fatty acids, gut microbiota-derived bacterial fermentation products, regulate the size and function of the colonic Treg pool and protect against colitis in a Ffar2-dependent manner in mice. Our study reveals that a class of abundant microbial metabolites underlies adaptive immune microbiota coadaptation and promotes colonic homeostasis and health.
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              Metabolites produced by commensal bacteria promote peripheral regulatory T cell generation

              Nicholas Arpaia, Clarissa Campbell, Xiying Fan … (2014)
              Intestinal microbes provide multicellular hosts with nutrients and confer resistance to infection. The delicate balance between pro- and anti-inflammatory mechanisms, essential for gut immune homeostasis, is affected by the composition of the commensal microbial community. Regulatory T (Treg) cells expressing transcription factor Foxp3 play a key role in limiting inflammatory responses in the intestine 1 . Although specific members of the commensal microbial community have been found to potentiate the generation of anti-inflammatory Treg or pro-inflammatory Th17 cells 2-6 , the molecular cues driving this process remain elusive. Considering the vital metabolic function afforded by commensal microorganisms, we hypothesized that their metabolic by-products are sensed by cells of the immune system and affect the balance between pro- and anti-inflammatory cells. We found that a short-chain fatty acid (SCFA), butyrate, produced by commensal microorganisms during starch fermentation, facilitated extrathymic generation of Treg cells. A boost in Treg cell numbers upon provision of butyrate was due to potentiation of extrathymic differentiation of Treg cells as the observed phenomenon was dependent upon intronic enhancer CNS1, essential for extrathymic, but dispensable for thymic Treg cell differentiation 1, 7 . In addition to butyrate, de novo Treg cell generation in the periphery was potentiated by propionate, another SCFA of microbial origin capable of HDAC inhibition, but not acetate, lacking this activity. Our results suggest that bacterial metabolites mediate communication between the commensal microbiota and the immune system, affecting the balance between pro- and anti-inflammatory mechanisms.
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                Author and article information

                Contributors
                Xinping Song: Role: InvestigationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Jing Lao: Role: InvestigationRole: Supervision
                Lulu Wang: Role: Writing – review & editing
                Sixi Liu:
                ORCID: https://orcid.org/0000-0003-1674-2685
                Role: Writing – review & editing
                Journal
                Journal ID (nlm-ta): Ther Adv Hematol
                Journal ID (iso-abbrev): Ther Adv Hematol
                Journal ID (publisher-id): TAH
                Journal ID (hwp): sptah
                Title: Therapeutic Advances in Hematology
                Publisher: SAGE Publications (Sage UK: London, England )
                ISSN (Print): 2040-6207
                ISSN (Electronic): 2040-6215
                Publication date (Electronic): 28 March 2024
                Publication date Collection: 2024
                Volume: 15
                Electronic Location Identifier: 20406207241237602
                Affiliations
                [1-20406207241237602]Shenzhen Children’s Hospital, China Medical University, Shenzhen, Guangdong 518026, China
                [2-20406207241237602]Shenzhen Children’s Hospital, China Medical University, Shenzhen, Guangdong 518026, China
                [3-20406207241237602]Department of Hematology and Oncology, Shenzhen Children’s Hospital, 7019 Yitian Road, Futian District, Shenzhen, Guangdong 518026, China
                [4-20406207241237602]Department of Hematology and Oncology, Shenzhen Children’s Hospital, 7019 Yitian Road, Futian District, Shenzhen, Guangdong 518026, China
                Author notes
                Author information
                https://orcid.org/0000-0003-1674-2685
                Article
                Publisher ID: 10.1177_20406207241237602
                DOI: 10.1177/20406207241237602
                PMC ID: 10979536
                PubMed ID: 38558826
                SO-VID: cce29f8a-8da1-45aa-9618-98e71f28b9f9
                Copyright © © The Author(s), 2024
                License:

                This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License ( https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages ( https://us.sagepub.com/en-us/nam/open-access-at-sage).

                History
                Date received : 6 November 2023
                Date accepted : 19 February 2024
                Funding
                Funded by: The Medical Science and Technology Foundation of Guangdong Province, ;
                Award ID: A2023335
                Funded by: Shenzhen Healthcare Research Project, ;
                Award ID: SZLY2018015
                Funded by: Sanming Project of Medicine in Shenzhen, ;
                Award ID: SZSM201512033
                Funded by: Shenzhen Key Medical Discipline Construction Fund, ;
                Award ID: SZXK034
                Funded by: Shenzhen Fund for Guangdong Provincial High-level Clinical Key Specialties, ;
                Award ID: SZGSP012
                Funded by: Guangdong Medical Science and Technology Research Project, ;
                Award ID: A2020101
                Categories
                Subject: Review
                Custom metadata
                cover-date January-December 2024
                typesetter ts1

                ScienceOpen disciplines: Hematology
                Keywords: acute graft-versus-host disease,allogeneic hematopoietic stem-cell transplantation,short-chain fatty acids
                Data availability:
                ScienceOpen disciplines: Hematology
                Keywords: acute graft-versus-host disease, allogeneic hematopoietic stem-cell transplantation, short-chain fatty acids

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