Articles producció científica> Ciències Mèdiques Bàsiques

The Gut Microbiota Metabolite Succinate Promotes Adipose Tissue Browning in Crohn's Disease

  • Identification data

    Identifier: imarina:9266842
    Authors:
    Monfort-Ferre, DiandraCaro, AleidisMenacho, MargaritaMarti, MarcEspina, BeatrizBoronat-Toscano, AlbertNunez-Roa, CatiSeco, JesusBautista, MichelleEspin, EloyMegia, AnaVendrell, JoanFernandez-Veledo, SoniaSerena, Carolina
    Abstract:
    Background and Aims Crohn's disease [CD] is associated with complex microbe-host interactions, involving changes in microbial communities, and gut barrier defects, leading to the translocation of microorganisms to surrounding adipose tissue [AT]. We evaluated the presence of beige AT depots in CD and questioned whether succinate and/or bacterial translocation promotes white-to-beige transition in adipocytes. Methods Visceral [VAT] and subcutaneous [SAT] AT biopsies, serum and plasma were obtained from patients with active [n = 21] or inactive [n = 12] CD, and from healthy controls [n = 15]. Adipose-derived stem cells [ASCs] and AT macrophages [ATMs] were isolated from VAT biopsies. Results Plasma succinate levels were significantly higher in patients with active CD than in controls and were intermediate in those with inactive disease. Plasma succinate correlated with the inflammatory marker high-sensitivity C-reactive protein. Expression of the succinate receptor SUCNR1 was higher in VAT, ASCs and ATMs from the active CD group than from the inactive or control groups. Succinate treatment of ASCs elevated the expression of several beige AT markers from controls and from patients with inactive disease, including uncoupling protein-1 [UCP1]. Notably, beige AT markers were prominent in ASCs from patients with active CD. Secretome profiling revealed that ASCs from patients with active disease secrete beige AT-related proteins, and co-culture assays showed that bacteria also trigger the white-to-beige switch of ASCs from patients with CD. Finally, AT depots from patients with CD exhibited a conversion from white to beige AT together with high UCP1 expression, which was corroborated by in situ thermal imaging analysis. Conclusions Succinate and bacteria trigger white-to-beige
  • Others:

    Author, as appears in the article.: Monfort-Ferre, Diandra; Caro, Aleidis; Menacho, Margarita; Marti, Marc; Espina, Beatriz; Boronat-Toscano, Albert; Nunez-Roa, Cati; Seco, Jesus; Bautista, Michelle; Espin, Eloy; Megia, Ana; Vendrell, Joan; Fernandez-Veledo, Sonia; Serena, Carolina;
    Department: Ciències Mèdiques Bàsiques
    URV's Author/s: Boronat Toscano, Albert / Fernandez Veledo, Sonia / Megía Colet, Ana / Monfort Ferre, Diandra / Serena Perelló, Carolina / Vendrell Ortega, Juan José
    Keywords: Triggers Sucnr1 Succinic acid Stem-cells Obesity Immune properties Gpr91 Extracellular succinate Creeping fat Beige fat Beige adipose tissue Bacteria translocation
    Abstract: Background and Aims Crohn's disease [CD] is associated with complex microbe-host interactions, involving changes in microbial communities, and gut barrier defects, leading to the translocation of microorganisms to surrounding adipose tissue [AT]. We evaluated the presence of beige AT depots in CD and questioned whether succinate and/or bacterial translocation promotes white-to-beige transition in adipocytes. Methods Visceral [VAT] and subcutaneous [SAT] AT biopsies, serum and plasma were obtained from patients with active [n = 21] or inactive [n = 12] CD, and from healthy controls [n = 15]. Adipose-derived stem cells [ASCs] and AT macrophages [ATMs] were isolated from VAT biopsies. Results Plasma succinate levels were significantly higher in patients with active CD than in controls and were intermediate in those with inactive disease. Plasma succinate correlated with the inflammatory marker high-sensitivity C-reactive protein. Expression of the succinate receptor SUCNR1 was higher in VAT, ASCs and ATMs from the active CD group than from the inactive or control groups. Succinate treatment of ASCs elevated the expression of several beige AT markers from controls and from patients with inactive disease, including uncoupling protein-1 [UCP1]. Notably, beige AT markers were prominent in ASCs from patients with active CD. Secretome profiling revealed that ASCs from patients with active disease secrete beige AT-related proteins, and co-culture assays showed that bacteria also trigger the white-to-beige switch of ASCs from patients with CD. Finally, AT depots from patients with CD exhibited a conversion from white to beige AT together with high UCP1 expression, which was corroborated by in situ thermal imaging analysis. Conclusions Succinate and bacteria trigger white-to-beige AT transition in CD. Understanding the role of beige AT in CD might aid in the development of therapeutic or diagnostic interventions.
    Thematic Areas: Saúde coletiva Nutrição Medicine (miscellaneous) Medicine (all) Medicina iii Medicina ii Medicina i General medicine Gastroenterology & hepatology Gastroenterology Engenharias ii Ciências biológicas ii Ciências biológicas i Ciências ambientais
    licence for use: https://creativecommons.org/licenses/by/3.0/es/
    Author's mail: carolina.serena@urv.cat albert.boronat@estudiants.urv.cat diandra.monfort@estudiants.urv.cat sonia.fernandez@urv.cat ana.megia@urv.cat juanjose.vendrell@urv.cat
    Author identifier: 0000-0003-3832-4249 0000-0003-2906-3788 0000-0002-5101-9452 0000-0002-6994-6115
    Record's date: 2024-09-07
    Papper version: info:eu-repo/semantics/publishedVersion
    Link to the original source: https://academic.oup.com/ecco-jcc/article/16/10/1571/6585018?login=false
    Licence document URL: https://repositori.urv.cat/ca/proteccio-de-dades/
    Papper original source: Journal Of Crohns & Colitis. 16 (10): 1571-1583
    APA: Monfort-Ferre, Diandra; Caro, Aleidis; Menacho, Margarita; Marti, Marc; Espina, Beatriz; Boronat-Toscano, Albert; Nunez-Roa, Cati; Seco, Jesus; Bautis (2022). The Gut Microbiota Metabolite Succinate Promotes Adipose Tissue Browning in Crohn's Disease. Journal Of Crohns & Colitis, 16(10), 1571-1583. DOI: 10.1093/ecco-jcc/jjac069
    Article's DOI: 10.1093/ecco-jcc/jjac069
    Entity: Universitat Rovira i Virgili
    Journal publication year: 2022
    Publication Type: Journal Publications
  • Keywords:

    Gastroenterology,Gastroenterology & Hepatology,Medicine (Miscellaneous)
    Triggers
    Sucnr1
    Succinic acid
    Stem-cells
    Obesity
    Immune properties
    Gpr91
    Extracellular succinate
    Creeping fat
    Beige fat
    Beige adipose tissue
    Bacteria translocation
    Saúde coletiva
    Nutrição
    Medicine (miscellaneous)
    Medicine (all)
    Medicina iii
    Medicina ii
    Medicina i
    General medicine
    Gastroenterology & hepatology
    Gastroenterology
    Engenharias ii
    Ciências biológicas ii
    Ciências biológicas i
    Ciências ambientais
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