Clostridium butyricum upregulates GPR109A/AMPK/PGC-1α and ameliorates acute pancreatitis-associated intestinal barrier injury in mice.

التفاصيل البيبلوغرافية
العنوان:	Clostridium butyricum upregulates GPR109A/AMPK/PGC-1α and ameliorates acute pancreatitis-associated intestinal barrier injury in mice.
المؤلفون:	Deng G; Department of Gastroenterology, The Second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, 510180, China., Wen B; Department of Gastroenterology, The Second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, 510180, China., Jia L; Department of Gastroenterology, The Second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, 510180, China. 16623111956@163.com., Liu J; Department of Gastroenterology, The Second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, 510180, China., Yan Q; Department of Gastroenterology, The Second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, 510180, China.; Department of Gastroenterology, Guangzhou First People's Hospital, South China University of Technology, Guangzhou, 510180, China.
المصدر:	Archives of microbiology [Arch Microbiol] 2024 May 18; Vol. 206 (6), pp. 265. Date of Electronic Publication: 2024 May 18.
نوع المنشور:	Journal Article
اللغة:	English
بيانات الدورية:	Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 0410427 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-072X (Electronic) Linking ISSN: 03028933 NLM ISO Abbreviation: Arch Microbiol Subsets: MEDLINE
أسماء مطبوعة:	Original Publication: Berlin, New York, Springer-Verlag.
مواضيع طبية MeSH:	Clostridium butyricum/metabolism , Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha/metabolism , Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha/genetics , Receptors, G-Protein-Coupled/metabolism , Receptors, G-Protein-Coupled/genetics , Pancreatitis/metabolism , Pancreatitis/microbiology , Pancreatitis/pathology , AMP-Activated Protein Kinases/metabolism , AMP-Activated Protein Kinases/genetics , Disease Models, Animal*, Animals ; Mice ; Intestinal Mucosa/metabolism ; Intestinal Mucosa/microbiology ; Mice, Inbred C57BL ; Male ; Signal Transduction ; Up-Regulation
مستخلص:	Acute pancreatitis frequently causes intestinal barrier damage, which aggravates pancreatitis. Although Clostridium butyricum exerts anti-inflammatory and protective effects on the intestinal barrier during acute pancreatitis, the underlying mechanism is unclear. The G protein-coupled receptors 109 A (GPR109A) and adenosine monophosphate-activated protein kinase (AMPK)/ peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1α) signaling pathways can potentially influence the integrity of the intestinal barrier. Our study generated acute pancreatitis mouse models via intraperitoneal injection of cerulein and lipopolysaccharides. After intervention with Clostridium butyricum, the model mice showed reduced small intestinal and colonic intestinal barrier damage, dysbiosis amelioration, and increased GPR109A/AMPK/PGC-1α expression. In conclusion, Clostridium butyricum could improve pancreatic and intestinal inflammation and pancreatic injury, and relieve acute pancreatitis-induced intestinal barrier damage in the small intestine and colon, which may be associated with GPR109A/AMPK/PGC-1α. (© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)
References:	Beger H G, Bittner R (1986) Bacterial contamination of pancreatic necrosis. A prospective clinical study [J]. Gastroenterology 91(2):433–438. https://doi.org/10.1016/0016-5085(86)90579-2. (PMID: 10.1016/0016-5085(86)90579-23522342) Blad C C, Tang C, Offermanns S (2012) G protein-coupled receptors for energy metabolites as new therapeutic targets [J]. Nat Rev Drug Discov 11(8):603–619. https://doi.org/10.1038/nrd3777. (PMID: 10.1038/nrd377722790105) BOXHOORN L, VOERMANS R P, BOUWENSE SA et al (2020) Acute pancreatitis [J]. Lancet (London, England), 396(10252): 726 – 34. https://doi.org/10.1016/s0140-6736(20)31310-6. Cantó C, Gerhart-Hines Z, FEIGE J N et al (2009) AMPK regulates energy expenditure by modulating NAD + metabolism and SIRT1 activity [J]. Nature 458(7241):1056–1060. https://doi.org/10.1038/nature07813. (PMID: 10.1038/nature07813192625083616311) Capurso G, Zerboni G, Signoretti M et al (2012) Role of the gut barrier in acute pancreatitis [J]. J Clin Gastroenterol. https://doi.org/10.1097/MCG.0b013e3182652096 . 46 Suppl: S46-51. (PMID: 10.1097/MCG.0b013e318265209622955357) Chelakkot C, Ghim J, Ryu SH (2018) Exp Mol Med 50(8):1–9. https://doi.org/10.1038/s12276-018-0126-x . Mechanisms regulating intestinal barrier integrity and its pathological implications [J]. Chiu C J, Scott H J, Gurd F N (1970). Intestinal mucosal lesion in low-flow states. II. The protective effect of intraluminal glucose as energy substrate [J]. Archives of surgery (Chicago, Ill: 1960), 101(4): 484-8. https://doi.org/10.1001/archsurg.1970.01340280036010. CUNNINGHAM K E VINCENTG, SODHI C P et al (2016) Peroxisome proliferator-activated Receptor-γ Coactivator 1-α (PGC1α) protects against experimental murine colitis [J]. J Biol Chem 291(19):10184–10200. https://doi.org/10.1074/jbc.M115.688812. (PMID: 10.1074/jbc.M115.688812269691664858969) D’errico I SALVATOREL (2011) Peroxisome proliferator-activated receptor-gamma coactivator 1-alpha (PGC1alpha) is a metabolic regulator of intestinal epithelial cell fate [J]. Proc Natl Acad Sci USA 108(16):6603–6608. https://doi.org/10.1073/pnas.1016354108. (PMID: 10.1073/pnas.1016354108214672243081029) Elamin E E, Masclee A A, Dekker J et al (2013) Short-chain fatty acids activate AMP-activated protein kinase and ameliorate ethanol-induced intestinal barrier dysfunction in Caco-2 cell monolayers [J]. J Nutr 143(12):1872–1881. https://doi.org/10.3945/jn.113.179549. (PMID: 10.3945/jn.113.17954924132573) Glaubitz J, Wilden A, Frost F et al (2023) Activated regulatory T-cells promote duodenal bacterial translocation into necrotic areas in severe acute pancreatitis [J]. Gut 72(7):1355–1369. https://doi.org/10.1136/gutjnl-2022-327448. (PMID: 10.1136/gutjnl-2022-32744836631247) Guilloteau P, Martin L, Eeckhaut V, et al (2010) From the gut to the peripheral tissues: the multiple effects of butyrate [J]. Nutr Res Rev 23(2):366–384. https://doi.org/10.1017/s0954422410000247. (PMID: 10.1017/s095442241000024720937167) Guo W, Li W, Su Y et al (2021) GPR109A alleviate mastitis and enhances the blood milk barrier by activating AMPK/Nrf2 and autophagy [J]. Int J Biol Sci 17(15):4271–4284. https://doi.org/10.7150/ijbs.62380. (PMID: 10.7150/ijbs.62380348034978579459) Hagihara M, KUROKI Y, ARIYOSHI T et al (2020) Clostridium butyricum modulates the Microbiome to protect intestinal barrier function in mice with antibiotic-Induced dysbiosis [J]. iScience 23(1):100772. https://doi.org/10.1016/j.isci.2019.100772. (PMID: 10.1016/j.isci.2019.10077231954979) Hoque R, Mehal W Z (2015) Inflammasomes in pancreatic physiology and disease [J]. Am J Physiol Gastrointest Liver Physiol 308(8):G643–G651. https://doi.org/10.1152/ajpgi.00388.2014. (PMID: 10.1152/ajpgi.00388.2014257000814398840) Jäger S, Handschin C, St-Pierre J et al (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha [J]. Proc Natl Acad Sci USA 104(29):12017–12022. https://doi.org/10.1073/pnas.0705070104. (PMID: 10.1073/pnas.0705070104176093681924552) Jin M, Zhang H, Wu M et al (2022) Colonic interleukin-22 protects intestinal mucosal barrier and microbiota abundance in severe acute pancreatitis [J]. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 36(3):e22174. https://doi.org/10.1096/fj.202101371R. Kim MS, Shigenaga J K, Moser A H et al (2005) Suppression of estrogen-related receptor alpha and medium-chain acyl-coenzyme A dehydrogenase in the acute-phase response [J]. J Lipid Res 46(10):2282–2288. https://doi.org/10.1194/jlr.M500217-JLR200. (PMID: 10.1194/jlr.M500217-JLR20016061943) Kuo W T, Odenwald M A, Turner J R et al (2022) Tight junction proteins occludin and ZO-1 as regulators of epithelial proliferation and survival [J]. Ann N Y Acad Sci 1514(1):21–33. https://doi.org/10.1111/nyas.14798. (PMID: 10.1111/nyas.14798355809949427709) Lei Y, Tang L, Liu S et al (2021) Parabacteroides produces acetate to alleviate heparanase-exacerbated acute pancreatitis through reducing neutrophil infiltration [J]. Microbiome 9(1):115. https://doi.org/10.1186/s40168-021-01065-2. (PMID: 10.1186/s40168-021-01065-2340161638138927) Lerch MM, Gorelick FS (2013) Models of acute and chronic pancreatitis [J]. Gastroenterology 144(6):1180–1193. https://doi.org/10.1053/j.gastro.2012.12.043. (PMID: 10.1053/j.gastro.2012.12.04323622127) Lesina M, Wörmann SM, Neuhöfer P et al (2014) Interleukin-6 in inflammatory and malignant diseases of the pancreas [J]. Semin Immunol 26(1):80–87. https://doi.org/10.1016/j.smim.2014.01.002. (PMID: 10.1016/j.smim.2014.01.00224572992) Li Z, Mccafferty K J, JUDD RL (2021) Role of HCA(2) in regulating intestinal homeostasis and suppressing Colon carcinogenesis [J]. Front Immunol 12:606384. https://doi.org/10.3389/fimmu.2021.606384. (PMID: 10.3389/fimmu.2021.606384337082037940178) Li H, Sun J, Du J et al (2018) Clostridium butyricum exerts a neuroprotective effect in a mouse model of traumatic brain injury via the gut-brain axis [J]. Neurogastroenterol Motil 30(5):e13260. https://doi.org/10.1111/nmo.13260. (PMID: 10.1111/nmo.1326029193450) Li X, Jamal M, Guo P, Biomedicine et al (2019) Pharmacotherapy = Biomedecine Pharmacotherapie 118:109363. https://doi.org/10.1016/j.biopha.2019.109363. (PMID: 10.1016/j.biopha.2019.109363) Li X Y, He C, Zhu Y et al (2020) Role of gut microbiota on intestinal barrier function in acute pancreatitis [J]. World J Gastroenterol 26(18):2187–2193. https://doi.org/10.3748/wjg.v26.i18.2187. (PMID: 10.3748/wjg.v26.i18.2187324767857235204) Li Z R Pengl, Green RS et al (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers [J]. J Nutr 139(9):1619–1625. https://doi.org/10.3945/jn.109.104638. (PMID: 10.3945/jn.109.104638) Ma X, Fan P X, Li LS et al (2012) Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions [J]. J Anim Sci 90(Suppl 4):266–268. https://doi.org/10.2527/jas.50965. (PMID: 10.2527/jas.5096523365351) MA L, Shen Q, Lyu W et al (2022) Clostridium butyricum and its derived extracellular vesicles modulate gut homeostasis and ameliorate Acute Experimental colitis [J]. Microbiol Spectr 10(4):e0136822. https://doi.org/10.1128/spectrum.01368-22. (PMID: 10.1128/spectrum.01368-2235762770) Nguyen TD, Hållenius FF, Lin X et al (2020) Monobutyrin and Monovalerin affect brain short-chain fatty acid profiles and tight-Junction protein expression in ApoE-Knockout rats Fed High-Fat diets [J]. Nutrients 12(4). https://doi.org/10.3390/nu12041202. Niu Panll, FANG W (2019) Mol Nutr Food Res 63(13):e1801419. https://doi.org/10.1002/mnfr.201801419 . X, et al. Clostridium butyricum Strains Suppress Experimental Acute Pancreatitis by Maintaining Intestinal Homeostasis [J]. Piao X, Liu B, Sui X et al (2020) Picroside II Improves Severe Acute Pancreatitis-Induced Intestinal Barrier Injury by Inactivating Oxidative and Inflammatory TLR4-Dependent PI3K/AKT/NF-κB Signaling and Improving Gut Microbiota [J]. Oxidative medicine and cellular longevity, 2020: 3589497. https://doi.org/10.1155/2020/3589497. Rowart P, Wu J, Caplan M J et al (2018) Implications of AMPK in the formation of epithelial tight junctions [J]. Int J Mol Sci 19(7). https://doi.org/10.3390/ijms19072040. Schwarz M, Thomsen J, Meyer H et al (2000) Frequency and time course of pancreatic and extrapancreatic bacterial infection in experimental acute pancreatitis in rats [J]. Surgery 127(4):427–432. https://doi.org/10.1067/msy.2000.104116. (PMID: 10.1067/msy.2000.10411610776434) Shimizu T, Shiratori K, Sawada T et al (2000) Recombinant human interleukin-11 decreases severity of acute necrotizing pancreatitis in mice [J]. Pancreas 21(2):134–140. https://doi.org/10.1097/00006676-200008000-00005. (PMID: 10.1097/00006676-200008000-0000510975706) Singh N, Gurav A, Sivaprakasam S et al (2014) Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis [J]. Immunity 40(1):128–139. https://doi.org/10.1016/j.immuni.2013.12.007. (PMID: 10.1016/j.immuni.2013.12.007244126174305274) Stoeva M K, Garcia-So J, Justice N et al (2021) Butyrate-producing human gut symbiont, Clostridium butyricum, and its role in health and disease [J]. Gut Microbes 13(1):1–28. https://doi.org/10.1080/19490976.2021.1907272. (PMID: 10.1080/19490976.2021.190727233874858) Sun Y Y, Li M, Li YY et al (2018) The effect of Clostridium butyricum on symptoms and fecal microbiota in diarrhea-dominant irritable bowel syndrome: a randomized, double-blind, placebo-controlled trial [J]. Sci Rep 8(1):2964. https://doi.org/10.1038/s41598-018-21241-z. (PMID: 10.1038/s41598-018-21241-z) Thangaraju M, Cresci G A, Liu K et al (2009) GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon [J]. Cancer Res 69(7):2826–2832. https://doi.org/10.1158/0008-5472.Can-08-4466. (PMID: 10.1158/0008-5472.Can-08-4466192763433747834) Xiao Z, Liu L, Jin Y et al (2021a) Clostridium tyrobutyricum protects against LPS-Induced Colonic inflammation via IL-22 signaling in mice [J]. Nutrients 13(1). https://doi.org/10.3390/nu13010215. Xiao Z, Liu L, Pei X et al (2021b) A potential probiotic for Diarrhea: Clostridium tyrobutyricum protects against LPS-Induced Epithelial Dysfunction via IL-22 produced by Th17 cells in the ileum [J]. Front Immunol 12:758227. https://doi.org/10.3389/fimmu.2021.758227. (PMID: 10.3389/fimmu.2021.758227349170808670534) Xu RC, Miao W T, Xu JY et al (2022) Neuroprotective effects of Sodium Butyrate and Monomethyl Fumarate Treatment through GPR109A Modulation and Intestinal Barrier Restoration on PD mice [J]. Nutrients 14(19). https://doi.org/10.3390/nu14194163. Yan Q, Jia L, Wen B et al (2022) Clostridium butyricum protects against pancreatic and intestinal Injury after severe Acute pancreatitis via downregulation of MMP9 [J]. Front Pharmacol 13:919010. https://doi.org/10.3389/fphar.2022.919010. (PMID: 10.3389/fphar.2022.919010359240439342915) Yu S, Xiong Y, Xu J et al (2020) Identification of dysfunctional gut microbiota through rectal swab in patients with different severity of Acute pancreatitis [J]. Dig Dis Sci 65(11):3223–3237. https://doi.org/10.1007/s10620-020-06061-4. (PMID: 10.1007/s10620-020-06061-432076933) Zhang YJ, Wu Q (2021) Sulforaphane protects intestinal epithelial cells against lipopolysaccharide-induced injury by activating the AMPK/SIRT1/PGC-1ɑ pathway [J]. Bioengineered 12(1):4349–4360. https://doi.org/10.1080/21655979.2021.1952368. (PMID: 10.1080/21655979.2021.1952368343087698806682) Zhang X M, Zhang Z Y, Zhang C H et al (2018) Biomed Environ Sci: BES 31(1):81–86. https://doi.org/10.3967/bes2018.010 . Intestinal Microbial Community Differs between Acute Pancreatitis Patients and Healthy Volunteers [J]. Zhao HB, Yan Q Q Jial et al (2020) Effect of Clostridium butyricum and Butyrate on Intestinal Barrier functions: study of a rat model of severe Acute Pancreatitis with Intra-abdominal hypertension [J]. Front Physiol 11:561061. https://doi.org/10.3389/fphys.2020.561061. (PMID: 10.3389/fphys.2020.561061331925577658654) Zheng B, Cantley LC (2007) Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase [J]. Proc Natl Acad Sci USA 104(3):819–822. https://doi.org/10.1073/pnas.0610157104. (PMID: 10.1073/pnas.0610157104172045631783397) Zhu Y, He C, Li X et al (2019) Gut microbiota dysbiosis worsens the severity of acute pancreatitis in patients and mice [J]. J Gastroenterol 54(4):347–358. https://doi.org/10.1007/s00535-018-1529-0. (PMID: 10.1007/s00535-018-1529-030519748) Zhu Y, Mei Q, Fu Y, Biomedicine et al (2021) Pharmacotherapy = Biomedecine Pharmacotherapie 141:111850. https://doi.org/10.1016/j.biopha.2021.111850. (PMID: 10.1016/j.biopha.2021.111850)
معلومات مُعتمدة:	81870438 the National Natural Science Foundation of China; NO.2022A1515010321 the National Natural Science Foundation of Guangdong Province; 202102020099 the Guangzhou Technology Projects
فهرسة مساهمة:	Keywords: Clostridium butyricum; AMPK; Acute pancreatitis; GPR109A; PGC-1α
المشرفين على المادة:	0 (Ppargc1a protein, mouse) 0 (Hcar2 protein, mouse)
تواريخ الأحداث:	Date Created: 20240518 Date Completed: 20240518 Latest Revision: 20240617
رمز التحديث:	20240617
DOI:	10.1007/s00203-024-04001-8
PMID:	38761195
قاعدة البيانات:	MEDLINE

Find this article in full text from Springer Verlag.

Full Text Finder

الوصف
تدمد:	1432-072X
DOI:	10.1007/s00203-024-04001-8