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Research Paper

Microbiota-derived I3A protects the intestine against radiation injury by activating AhR/IL-10/Wnt signaling and enhancing the abundance of probiotics

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Article: 2347722 | Received 01 Oct 2023, Accepted 22 Apr 2024, Published online: 05 May 2024

References

  • Hauer-Jensen M, Denham JW, Andreyev HJ. Radiation enteropathy—pathogenesis, treatment and prevention. Nat Rev Gastroenterol Hepatol. 2014;11(8):470–23. doi:10.1038/nrgastro.2014.46.
  • Li H, Kucharavy HC, Hajj C, Zhao L, Hua G, Glass R, Paty PB, Fuks Z, Kolesnick R, Hubbard K. et al. Radiation-induced gastrointestinal (GI) syndrome as a function of age. Cell Death Discov. 2023;9(1):31. doi:10.1038/s41420-023-01298-0.
  • Wang K, Tepper JE. Radiation therapy-associated toxicity: etiology, management, and prevention. CA Cancer J Clin. 2021;71(5):437–454. doi:10.3322/caac.21689.
  • Garg M, Jones RM, Vaughan RB, Testro AG. Intestinal transplantation: current status and future directions. J Gastroenterol Hepatol. 2011;26(8):1221–1228. doi:10.1111/j.1440-1746.2011.06783.x.
  • Chelakkot C, Ghim J, Ryu SH. Mechanisms regulating intestinal barrier integrity and its pathological implications. Experimental & Molecular Medicine. 2018;50(8):1–9. doi:10.1038/s12276-018-0126-x.
  • Ciorba MA, Riehl TE, Rao MS, Moon C, Ee X, Nava GM, Walker MR, Marinshaw JM, Stappenbeck TS, Stenson WF. et al. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut. 2012;61(6):829–838. doi:10.1136/gutjnl-2011-300367.
  • Riehl TE, Alvarado D, Ee X, Zuckerman A, Foster L, Kapoor V, Thotala D, Ciorba MA, Stenson WF. Lactobacillus rhamnosus GG protects the intestinal epithelium from radiation injury through release of lipoteichoic acid, macrophage activation and the migration of mesenchymal stem cells. Gut. 2019;68(6):1003–1013. doi:10.1136/gutjnl-2018-316226.
  • Ding X, Li Q, Li P, Chen X, Xiang L, Bi L, Zhu J, Huang X, Cui B, Zhang F. et al. Fecal microbiota transplantation: a promising treatment for radiation enteritis? Radiother Oncol. 2020;143:12–18. doi:10.1016/j.radonc.2020.01.011.
  • Suez J, Zmora N, Segal E, Elinav E. The pros, cons, and many unknowns of probiotics. Nat Med. 2019;25(5):716–729. doi:10.1038/s41591-019-0439-x.
  • Oliphant K, Allen-Vercoe E. Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health. Microbiome. 2019;7(1):91. doi:10.1186/s40168-019-0704-8.
  • Liu D, Zhuang B, Wei M, Yuan T, Li J, Deng P, Du L, Yuan B, Jin Y. Oral konjac glucomannan for prevention of ionizing radiation-induced injury by regulating gut microbiota and increasing short chain fatty acids. Int J Biol Macromol. 2023;240:124402. doi:10.1016/j.ijbiomac.2023.124402.
  • Guo L, Da F, Gao Q, Miao X, Guo J, Zhang W, Li J, Wang J, Liu J. Irradiation-induced intestinal injury is associated with disorders of bile acids metabolism. Int J Radiat Oncol Biol Phys. 2023;115(2):490–500. doi:10.1016/j.ijrobp.2022.08.007.
  • Li Y, Xiao H, Dong J, Luo D, Wang H, Zhang S, Zhu T, Zhu C, Cui M, Fan S. et al. Gut microbiota metabolite fights against dietary polysorbate 80-aggravated radiation enteritis. Front Microbiol. 2020;11:1450. doi:10.3389/fmicb.2020.01450.
  • Li Y, Dong J, Xiao H, Zhang S, Wang B, Cui M, Fan S. Gut commensal derived-valeric acid protects against radiation injuries. Gut Microbes. 2020;11(4):789–806. doi:10.1080/19490976.2019.1709387.
  • Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe. 2018;23(6):716–724. doi:10.1016/j.chom.2018.05.003.
  • Roager HM, Licht TR. Microbial tryptophan catabolites in health and disease. Nat Commun. 2018;9(1):3294. doi:10.1038/s41467-018-05470-4.
  • Singh VK, Seed TM, Cheema AK. Metabolomics-based predictive biomarkers of radiation injury and countermeasure efficacy: current status and future perspectives. Expert Rev Mol Diagn. 2021;21(7):641–654. doi:10.1080/14737159.2021.1933448.
  • Xiao HW, Cui M, Li Y, Dong JL, Zhang SQ, Zhu CC, Jiang M, Zhu T, Wang B, Wang H-C. et al. Gut microbiota-derived indole 3-propionic acid protects against radiation toxicity via retaining acyl-CoA-binding protein. Microbiome. 2020;8(1):69. doi:10.1186/s40168-020-00845-6.
  • Guo H, Chou WC, Lai Y, Liang K, Tam JW, Brickey WJ, Chen L, Montgomery ND, Li X, Bohannon LM. et al. Multi-omics analyses of radiation survivors identify radioprotective microbes and metabolites. Science. 2020;370(6516):370. doi:10.1126/science.aay9097.
  • Puccetti M, Gomes Dos Reis L, Pariano M, Costantini C, Renga G, Ricci M, Traini D, Giovagnoli S. Development and in vitro-in vivo performances of an inhalable indole-3-carboxaldehyde dry powder to target pulmonary inflammation and infection. Int J Pharm. 2021;607:121004. doi:10.1016/j.ijpharm.2021.121004.
  • Powell DN, Swimm A, Sonowal R, Bretin A, Gewirtz AT, Jones RM, Kalman D. Indoles from the commensal microbiota act via the AHR and IL-10 to tune the cellular composition of the colonic epithelium during aging. Proc Natl Acad Sci U S A. 2020;117(35):21519–21526. doi:10.1073/pnas.2003004117.
  • Stockinger B, Shah K, Wincent E. AHR in the intestinal microenvironment: safeguarding barrier function. Nat Rev Gastroenterol Hepatol. 2021;18(8):559–570. doi:10.1038/s41575-021-00430-8.
  • Naganuma M, Sugimoto S, Mitsuyama K, Kobayashi T, Yoshimura N, Ohi H, Tanaka S, Andoh A, Ohmiya N, Saigusa K. et al. Efficacy of Indigo Naturalis in a multicenter randomized controlled trial of patients with ulcerative colitis. Gastroenterology. 2018;154(4):935–947. doi:10.1053/j.gastro.2017.11.024.
  • Guan D, Yang Y, Pang M, Liu X, Li Y, Huang P, Shang H, Wei H, Ye Z. Indole-3-carboxaldehyde ameliorates ionizing radiation-induced hematopoietic injury by enhancing hematopoietic stem and progenitor cell quiescence. Mol Cell Biochem. 2024;479(2):313–323. doi:10.1007/s11010-023-04732-0.
  • Metcalfe C, Kljavin NM, Ybarra R, de Sauvage FJ. Lgr5+ stem cells are indispensable for radiation-induced intestinal regeneration. Cell Stem Cell. 2014;14(2):149–159. doi:10.1016/j.stem.2013.11.008.
  • Schwiebs A, Faqar-Uz-Zaman F, Herrero San Juan M, Radeke HH. S1P lyase regulates intestinal stem cell quiescence via ki-67 and FOXO3. Int J Mol Sci. 2021;22(11):22. doi:10.3390/ijms22115682.
  • Yu S, Balasubramanian I, Laubitz D, Tong K, Bandyopadhyay S, Lin X, Flores J, Singh R, Liu Y, Macazana C. et al. Paneth cell-derived lysozyme defines the composition of mucolytic microbiota and the inflammatory tone of the intestine. Immunity. 2020;53(2):398–416.e8. doi:10.1016/j.immuni.2020.07.010.
  • Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009;9(11):799–809. doi:10.1038/nri2653.
  • Shen L, Weber CR, Raleigh DR, Yu D, Turner JR. Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol. 2011;73(1):283–309. doi:10.1146/annurev-physiol-012110-142150.
  • Ganapathy AS, Saha K, Wang A, Arumugam P, Dharmaprakash V, Yochum G, Koltun W, Nighot M, Perdew G, Thompson TA. et al. Alpha-tocopherylquinone differentially modulates claudins to enhance intestinal epithelial tight junction barrier via AhR and Nrf2 pathways. Cell Rep. 2023;42(7):112705. doi:10.1016/j.celrep.2023.112705.
  • Böttcher A, Büttner M, Tritschler S, Sterr M, Aliluev A, Oppenländer L, Burtscher I, Sass S, Irmler M, Beckers J. et al. Non-canonical Wnt/PCP signalling regulates intestinal stem cell lineage priming towards enteroendocrine and Paneth cell fates. Nat Cell Biol. 2021;23(1):23–31. doi:10.1038/s41556-020-00617-2.
  • Venkatesh M, Mukherjee S, Wang H, Li H, Sun K, Benechet AP, Qiu Z, Maher L, Redinbo M, Phillips R. et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity. 2014;41(2):296–310. doi:10.1016/j.immuni.2014.06.014.
  • Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, Verbeke K. et al. A decrease of the butyrate-producing species roseburia hominis and faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63(8):1275–1283. doi:10.1136/gutjnl-2013-304833.
  • Yu Y, Lin X, Feng F, Wei Y, Wei S, Gong Y, Guo C, Wang Q, Shuai P, Wang T. et al. Gut microbiota and ionizing radiation-induced damage: is there a link? Environ Res. 2023;229:115947. doi:10.1016/j.envres.2023.115947.
  • Ley S, Galuba O, Salathe A, Melin N, Aebi A, Pikiolek M, Knehr J, Carbone W, Beibel M, Nigsch F. et al. Screening of intestinal crypt organoids: a simple readout for complex biology. SLAS Discovery. 2017;22(5):571–582. doi:10.1177/2472555216683651.
  • Olcina MM, Giaccia AJ. Reducing radiation-induced gastrointestinal toxicity — the role of the PHD/HIF axis. J Clin Invest. 2016;126(10):3708–3715. doi:10.1172/JCI84432.
  • Fu G, Chen S, Liang L, Li X, Tang P, Rao X, Pan M, Xu X, Li Y, Yao Y. et al. SIRT1 inhibitors mitigate radiation-induced GI syndrome by enhancing intestinal-stem-cell survival. Cancer Lett. 2021;501:20–30. doi:10.1016/j.canlet.2020.12.034.
  • Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M. et al. Lgr5+ve Stem Cells Drive Self-Renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell. 2010;6(1):25–36. doi:10.1016/j.stem.2009.11.013.
  • Clevers HC, Bevins CL. Paneth cells: maestros of the small intestinal crypts. Annu Rev Physiol. 2013;75(1):289–311. doi:10.1146/annurev-physiol-030212-183744.
  • Kiela PR, Ghishan FK. Physiology of intestinal absorption and secretion. Best Pract Res Clin Gastroenterol. 2016;30(2):145–159. doi:10.1016/j.bpg.2016.02.007.
  • Renga G, Nunzi E, Pariano M, Puccetti M, Bellet MM, Pieraccini G, D’Onofrio F, Santarelli I, Stincardini C, Aversa F. et al. Optimizing therapeutic outcomes of immune checkpoint blockade by a microbial tryptophan metabolite. J Immunother Cancer. 2022;10(3):10. doi:10.1136/jitc-2021-003725.
  • Zhang R, Huang G, Ren Y, Wang H, Ye Y, Guo J, Wang M, Zhu W, Yu K. Effects of dietary indole-3-carboxaldehyde supplementation on growth performance, intestinal epithelial function, and intestinal microbial composition in weaned piglets. Front Nutr. 2022;9:896815. doi:10.3389/fnut.2022.896815.
  • Zhao TS, Xie LW, Cai S, Xu JY, Zhou H, Tang LF, Yang C, Fang S, Li M, Tian Y. et al. Dysbiosis of gut microbiota is associated with the progression of radiation-induced intestinal injury and is alleviated by oral compound probiotics in mouse Model. Front Cell Infect Microbiol. 2021;11:717636. doi:10.3389/fcimb.2021.717636.
  • Lee YS, Kim TY, Kim Y, Lee SH, Kim S, Kang SW, Yang J-Y, Baek I-J, Sung YH, Park Y-Y. et al. Microbiota-derived lactate accelerates intestinal stem-cell-mediated epithelial development. Cell Host Microbe. 2018;24(6):833–46.e6. doi:10.1016/j.chom.2018.11.002.
  • Jian YP, Yang G, Zhang LH, Liang JY, Zhou HL, Wang YS, Xu Z-X. Lactobacillus plantarum alleviates irradiation-induced intestinal injury by activation of FXR-FGF15 signaling in intestinal epithelia. J Cell Physiol. 2022;237(3):1845–1856. doi:10.1002/jcp.30651.
  • Delia P, Sansotta G, Donato V, Frosina P, Messina G, De Renzis C, Famularo G. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13(6):912–915. doi:10.3748/wjg.v13.i6.912.
  • Fite A, Macfarlane GT, Cummings JH, Hopkins MJ, Kong SC, Furrie E, Macfarlane S. Identification and quantitation of mucosal and faecal desulfovibrios using real time polymerase chain reaction. Gut. 2004;53(4):523–529. doi:10.1136/gut.2003.031245.
  • Belotserkovsky I, Sansonetti PJ. Shigella and Enteroinvasive Escherichia Coli. Curr Top Microbiol Immunol. 2018;416:1–26.
  • Liu X, Zhang X, Zhang J, Luo Y, Xu B, Ling S, Zhang Y, Li W, Yao X. Activation of aryl hydrocarbon receptor in Langerhans cells by a microbial metabolite of tryptophan negatively regulates skin inflammation. J Dermatol Sci. 2020;100(3):192–200. doi:10.1016/j.jdermsci.2020.10.004.
  • Scott SA, Fu J, Chang PV. Microbial tryptophan metabolites regulate gut barrier function via the aryl hydrocarbon receptor. Proc Natl Acad Sci U S A. 2020;117(32):19376–19387. doi:10.1073/pnas.2000047117.
  • Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell. 2012;149(6):1192–1205. doi:10.1016/j.cell.2012.05.012.
  • Saha S, Aranda E, Hayakawa Y, Bhanja P, Atay S, Brodin NP, Li J, Asfaha S, Liu L, Tailor Y. et al. Macrophage-derived extracellular vesicle-packaged WNTs rescue intestinal stem cells and enhance survival after radiation injury. Nat Commun. 2016;7(1):13096. doi:10.1038/ncomms13096.
  • Swafford D, Shanmugam A, Ranganathan P, Manoharan I, Hussein MS, Patel N, Sifuentes H, Koni PA, Prasad PD, Thangaraju M. et al. The wnt–β-Catenin–IL-10 signaling axis in intestinal APCs protects mice from Colitis-Associated colon cancer in response to gut microbiota. J Immunol. 2020;205(8):2265–2275. doi:10.4049/jimmunol.1901376.
  • Tennoune N, Andriamihaja M, Blachier F. Production of indole and indole-Related Compounds by the intestinal microbiota and consequences for the Host: the good, the bad, and the ugly. Microorganisms. 2022;10(5):10. doi:10.3390/microorganisms10050930.
  • Kaur K, Jaitak V. Recent development in Indole Derivatives as anticancer agents for breast cancer. Anticancer Agents Med Chem. 2019;19(8):962–983. doi:10.2174/1871520619666190312125602.
  • Han JX, Tao ZH, Wang JL, Zhang L, Yu CY, Kang ZR, Xie Y, Li J, Lu S, Cui Y. et al. Microbiota-derived tryptophan catabolites mediate the chemopreventive effects of statins on colorectal cancer. Nat Microbiol. 2023;8(5):919–933. doi:10.1038/s41564-023-01363-5.
  • Zhang Q, Zhao Q, Li T, Lu L, Wang F, Zhang H, Liu Z, Ma H, Zhu Q, Wang J. et al. Lactobacillus plantarum-derived indole-3-lactic acid ameliorates colorectal tumorigenesis via epigenetic regulation of CD8+ T cell immunity. Cell Metab. 2023;35(6):943–60.e9. doi:10.1016/j.cmet.2023.04.015.
  • Nejman D, Livyatan I, Fuks G, Gavert N, Zwang Y, Geller LT, Rotter-Maskowitz A, Weiser R, Mallel G, Gigi E. et al. The human tumor microbiome is composed of tumor type–specific intracellular bacteria. Science. 2020;368(6494):973–980. doi:10.1126/science.aay9189.
  • Kalaora S, Nagler A, Nejman D, Alon M, Barbolin C, Barnea E, Ketelaars SLC, Cheng K, Vervier K, Shental N. et al. Identification of bacteria-derived HLA-bound peptides in melanoma. Nature. 2021;592(7852):138–143. doi:10.1038/s41586-021-03368-8.
  • Li M, Gu MM, Lang Y, Shi J, Chen BPC, Guan H, Yu L, Zhou P-K, Shang Z-F. The vanillin derivative VND3207 protects intestine against radiation injury by modulating p53/NOXA signaling pathway and restoring the balance of gut microbiota. Free Radic Biol Med. 2019;145:223–236. doi:10.1016/j.freeradbiomed.2019.09.035.
  • Varghese F, Bukhari AB, Malhotra R, De A, Aziz SA. IHC profiler: an open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PloS One. 2014;9(5):e96801. doi:10.1371/journal.pone.0096801.
  • Xie LW, Cai S, Zhao TS, Li M, Tian Y. Green tea derivative (-)-epigallocatechin-3-gallate (EGCG) confers protection against ionizing radiation-induced intestinal epithelial cell death both in vitro and in vivo. Free Radic Biol Med. 2020;161:175–186. doi:10.1016/j.freeradbiomed.2020.10.012.