120
Views
0
CrossRef citations to date
0
Altmetric
Review

Gut Microbiota and Epigenetics in Colorectal Cancer: Implications for Carcinogenesis and Therapeutic Intervention

& ORCID Icon
Pages 403-418 | Received 30 Oct 2023, Accepted 24 Jan 2024, Published online: 27 Feb 2024

References

  • El-Salhy M , HatlebakkJG, GiljaOH, BråthenKristoffersen A, HauskenT. Efficacy of faecal microbiota transplantation for patients with irritable bowel syndrome in a randomised, double-blind, placebo-controlled study. Gut69(5), 859–867 (2020).
  • Chhikara BS , ParangK. Global Cancer Statistics 2022: the trends projection analysis. Chem. Biol. Lett.10(1), 451, 1–16 (2023).
  • Wild CP . Complementing the genome with an ‘exposome’: the outstanding challenge of environmental exposure measurement in molecular epidemiology. Cancer Epidemiol. Biomarkers Prev.14(8), 1847–1850 (2005).
  • Hillman ET , LuH, YaoT, NakatsuCH. Microbial ecology along the gastrointestinal tract. Microbes Environ.32(4), 300–313 (2017).
  • Rinninella E , RaoulP, CintoniMet al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms7(1), 14, 1–22 (2019).
  • Carding S , VerbekeK, VipondDT, CorfeBM, OwenLJ. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis.26, 26191 (2015).
  • Hrncir T . Gut microbiota dysbiosis: triggers, consequences, diagnostic and therapeutic options. Microorganisms10(3), 578 (2022).
  • Zhao L-Y , MeiJ-X, YuGet al. Role of the gut microbiota in anticancer therapy: from molecular mechanisms to clinical applications. Signal Transduct. Target. Ther.8(1), 201 (2023).
  • Yamamoto Y , NakanishiY, MurakamiSet al. A metabolomic-based evaluation of the role of commensal microbiota throughout the gastrointestinal tract in mice. Microorganisms6(4), 101 (2018).
  • Saputo S , FaustoferriRC, QuiveyRGJ. Vitamin D compounds are bactericidal against Streptococcus mutans and target the bacitracin-associated efflux system. Antimicrob. Agents Chemother.62(1), 10–1128 (2018).
  • McFarland LV . Antibiotic-associated diarrhea: epidemiology, trends and treatment. Future Microbiol.3(5), 563–578 (2008).
  • Gouyer V , DubuquoyL, Robbe-MasselotCet al. Delivery of a mucin domain enriched in cysteine residues strengthens the intestinal mucous barrier. Sci. Rep.5, 9577 (2015).
  • Capelluto DGS . Tollip: a multitasking protein in innate immunity and protein trafficking. Microbes Infect.14(2), 140–147 (2012).
  • Kelly D , MulderIE. Microbiome and immunological interactions. Nutr. Rev.70(Suppl. 1), S18–S30 (2012).
  • Zhao Q , ElsonCO. Adaptive immune education by gut microbiota antigens. Immunology154(1), 28–37 (2018).
  • Jahani-Sherafat S , AlebouyehM, MoghimS, AhmadiAmoli H, Ghasemian-SafaeiH. Role of gut microbiota in the pathogenesis of colorectal cancer; a review article. Gastroenterol. Hepatol.11(2), 101–109 (2018).
  • Sobhani I , AmiotA, LeBaleur Yet al. Microbial dysbiosis and colon carcinogenesis: could colon cancer be considered a bacteria-related disease? Ther. Adv. Gastroenterol. 6(3), 215–229 (2013).
  • Lucas C , BarnichN, NguyenHTT. Microbiota, inflammation and colorectal cancer. Int. J. Mol. Sci.18(6), 1310 (2017).
  • Janakiram NB , RaoCV. The role of inflammation in colon cancer. Adv. Exp. Med. Biol.816, 25–52 (2014).
  • Ou J , CarboneroF, ZoetendalEGet al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am. J. Clin. Nutr.98(1), 111–120 (2013).
  • Rubinstein MR , WangX, LiuW, HaoY, CaiG, HanYW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe14(2), 195–206 (2013).
  • Casasanta MA , YooCC, UdayasuryanBet al. Fusobacterium nucleatum host-cell binding and invasion induces IL-8 and CXCL1 secretion that drives colorectal cancer cell migration. Sci. Signal.13(641), eaba9157 (2020).
  • Cougnoux A , DalmassoG, MartinezRet al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut63(12), 1932–1942 (2014).
  • Martin OCB , BergonziniA, D’AmicoFet al. Infection with genotoxin-producing Salmonella enterica synergises with loss of the tumour suppressor APC in promoting genomic instability via the PI3K pathway in colonic epithelial cells. Cell. Microbiol.21(12), e13099 (2019).
  • Wang X , HuyckeMM. Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology132(2), 551–561 (2007).
  • Huycke MM , MooreDR. In vivo production of hydroxyl radical by Enterococcus faecalis colonizing the intestinal tract using aromatic hydroxylation. Free Radic. Biol. Med.33(6), 818–826 (2002).
  • Huycke MM , MooreD, JoyceWet al. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol. Microbiol.42(3), 729–740 (2001).
  • Tsoi H , ChuESH, ZhangXet al. Peptostreptococcus anaerobius induces intracellular cholesterol biosynthesis in colon cells to induce proliferation and causes dysplasia in mice. Gastroenterology152(6), 1419–1433.e5 (2017).
  • Mancuso G , MidiriA, BiondoCet al. Bacteroides fragilis-derived lipopolysaccharide produces cell activation and lethal toxicity via toll-like receptor 4. Infect. Immun.73(9), 5620–5627 (2005).
  • Cheng WT , KantilalHK, DavamaniF. The mechanism of Bacteroides fragilis toxin contributes to colon cancer formation. Malays. J. Med. Sci.27(4), 9–21 (2020).
  • Hold GL , GarrettWS. Gut microbiota. Microbiota organization–a key to understanding CRC development. Nat. Rev. Gastroenterol. Hepatol.12(3), 128–129 (2015).
  • Niccolai E , RussoE, BaldiSet al. Significant and conflicting correlation of IL-9 with Prevotella and Bacteroides in human colorectal cancer. Front. Immunol.11, 573158 (2020).
  • Greer JB , O’KeefeSJ. Microbial induction of immunity, inflammation, and cancer. Front. Physiol.1, 168 (2011).
  • Vargas AJ , ThompsonPA. Diet and nutrient factors in colorectal cancer risk. Nutr. Clin. Pract. Off. Publ. Am. Soc. Parenter. Enter. Nutr.27(5), 613–623 (2012).
  • Walker AW , InceJ, DuncanSHet al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J.5(2), 220–230 (2011).
  • Louis P , YoungP, HoltropG, FlintHJ. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ. Microbiol.12(2), 304–314 (2010).
  • Chen H-M , YuY-N, WangJ-Let al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am. J. Clin. Nutr.97(5), 1044–1052 (2013).
  • Windey K , DePreter V, VerbekeK. Relevance of protein fermentation to gut health. Mol. Nutr. Food Res.56(1), 184–196 (2012).
  • Holliday R . Mechanisms for the control of gene activity during development. Biol. Rev. Camb. Philos. Soc.65(4), 431–471 (1990).
  • Luger K , MäderAW, RichmondRK, SargentDF, RichmondTJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature389(6648), 251–260 (1997).
  • Castillo J , López-RodasG, FrancoL. Histone post-translational modifications and nucleosome organisation in transcriptional regulation: some open questions. Adv. Exp. Med. Biol.966, 65–92 (2017).
  • Xie Y-H , ChenY-X, FangJ-Y. Comprehensive review of targeted therapy for colorectal cancer. Signal Transduct. Target. Ther.5(1), 22 (2020).
  • Kanwal R , GuptaS. Epigenetic modifications in cancer. Clin. Genet.81(4), 303–311 (2012).
  • Sun D , ChenY, FangJ-Y. Influence of the microbiota on epigenetics in colorectal cancer. Natl Sci. Rev.6(6), 1138–1148 (2018).
  • Hu S , LiuL, ChangEB, WangJ-Y, RaufmanJ-P. Butyrate inhibits pro-proliferative miR-92a by diminishing c-Myc-induced miR-17-92a cluster transcription in human colon cancer cells. Mol. Cancer14, 180 (2015).
  • Zullig LL , SmithVA, JacksonGLet al. Colorectal cancer statistics from the Veterans Affairs Central Cancer Registry. Clin. Colorectal Cancer15(4), e199–e204 (2016).
  • Kim SW . The role of microRNAs in colorectal cancer. Korean J. Gastroenterol.69(4), 206–211 (2017).
  • Gao P , TchernyshyovI, ChangT-Cet al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature458(7239), 762–765 (2009).
  • Yuan C , BurnsMB, SubramanianS, BlekhmanR. Interaction between host microRNAs and the gut microbiota in colorectal cancer. mSystems3(3), 10–1128 (2018).
  • Liu S , ChangW, JinYet al. The function of histone acetylation in cervical cancer development. Biosci. Rep.39(4), BSR20190527 (2019).
  • Legube G , TroucheD. Regulating histone acetyltransferases and deacetylases. EMBO Rep.4(10), 944–947 (2003).
  • Yuille S , ReichardtN, PandaS, DunbarH, MulderIE. Human gut bacteria as potent class I histone deacetylase inhibitors in vitro through production of butyric acid and valeric acid. PLOS ONE13(7), e0201073 (2018).
  • Takahashi K , SugiY, HosonoA, KaminogawaS. Epigenetic regulation of TLR4 gene expression in intestinal epithelial cells for the maintenance of intestinal homeostasis. J. Immunol.183(10), 6522–6529 (2009).
  • Chuang LSH , ItoY. RUNX3 is multifunctional in carcinogenesis of multiple solid tumors. Oncogene29(18), 2605–2615 (2010).
  • Ku J-L , KangS-B, ShinY-Ket al. Promoter hypermethylation downregulates RUNX3 gene expression in colorectal cancer cell lines. Oncogene23(40), 6736–6742 (2004).
  • Jones PA . Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet.13(7), 484–492 (2012).
  • Crider KS , YangTP, BerryRJ, BaileyLB. Folate and DNA methylation: a review of molecular mechanisms and the evidence for folate’s role. Adv. Nutr.3(1), 21–38 (2012).
  • Wasson GR , McGlynnAP, McNultyHet al. Global DNA and p53 region-specific hypomethylation in human colonic cells is induced by folate depletion and reversed by folate supplementation. J. Nutr.136(11), 2748–2753 (2006).
  • Ansari I , RaddatzG, GutekunstJet al. The microbiota programs DNA methylation to control intestinal homeostasis and inflammation. Nat. Microbiol.5(4), 610–619 (2020).
  • Feinberg AP , OhlssonR, HenikoffS. The epigenetic progenitor origin of human cancer. Nat. Rev. Genet.7(1), 21–33 (2006).
  • Feinberg AP , VogelsteinB. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature301(5895), 89–92 (1983).
  • Kaiko GE , RyuSH, KouesOIet al. The colonic crypt protects stem cells from microbiota-derived metabolites. Cell165(7), 1708–1720 (2016).
  • Gonneaud A , TurgeonN, BoudreauF, PerreaultN, RivardN, AsselinC. Distinct roles for intestinal epithelial cell-specific Hdac1 and Hdac2 in the regulation of murine intestinal homeostasis. J. Cell. Physiol.231(2), 436–448 (2016).
  • Tan M , LuoH, LeeSet al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell146(6), 1016–1028 (2011).
  • Wan J , LiuH, ChuJ, ZhangH. Functions and mechanisms of lysine crotonylation. J. Cell. Mol. Med.23(11), 7163–7169 (2019).
  • Fellows R , DenizotJ, StellatoCet al. Microbiota derived short chain fatty acids promote histone crotonylation in the colon through histone deacetylases. Nat. Commun.9(1), 105 (2018).
  • Maslowski KM , VieiraAT, NgAet al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature461(7268), 1282–1286 (2009).
  • Macia L , TanJ, VieiraATet al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun.6, 6734 (2015).
  • Liu L , LiL, MinJet al. Butyrate interferes with the differentiation and function of human monocyte-derived dendritic cells. Cell. Immunol.277(1–2), 66–73 (2012).
  • Vinolo MAR , RodriguesHG, FestucciaWTet al. Tributyrin attenuates obesity-associated inflammation and insulin resistance in high-fat-fed mice. Am. J. Physiol. Endocrinol. Metab.303(2), E272–E282 (2012).
  • Chang PV , HaoL, OffermannsS, MedzhitovR. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl Acad. Sci. USA111(6), 2247–2252 (2014).
  • Cox MA , JacksonJ, StantonMet al. Short-chain fatty acids act as antiinflammatory mediators by regulating prostaglandin E(2) and cytokines. World J. Gastroenterol.15(44), 5549–5557 (2009).
  • Zeng X , SunkaraLT, JiangWet al. Induction of porcine host defense peptide gene expression by short-chain fatty acids and their analogs. PLOS ONE8(8), e72922 (2013).
  • Millard AL , MertesPM, ItteletD, VillardF, JeannessonP, BernardJ. Butyrate affects differentiation, maturation and function of human monocyte-derived dendritic cells and macrophages. Clin. Exp. Immunol.130(2), 245–255 (2002).
  • Singh N , ThangarajuM, PrasadPDet al. Blockade of dendritic cell development by bacterial fermentation products butyrate and propionate through a transporter (Slc5a8)-dependent inhibition of histone deacetylases. J. Biol. Chem.285(36), 27601–27608 (2010).
  • Morinobu A , KannoY, O’SheaJJ. Discrete roles for histone acetylation in human T helper 1 cell-specific gene expression. J. Biol. Chem.279(39), 40640–40646 (2004).
  • Kespohl M , VachharajaniN, LuuMet al. The microbial metabolite butyrate induces expression of Th1-associated factors in CD4(+) T cells. Front. Immunol.8, 1036 (2017).
  • Chen L , SunM, WuWet al. Microbiota metabolite butyrate differentially regulates Th1 and Th17 cells’ differentiation and function in induction of colitis. Inflamm. Bowel Dis.25(9), 1450–1461 (2019).
  • Zhang M , ZhouQ, DorfmanRGet al. Butyrate inhibits interleukin-17 and generates Tregs to ameliorate colorectal colitis in rats. BMC Gastroenterol.16(1), 84 (2016).
  • Sekirov I , RussellSL, AntunesLCM, FinlayBB. Gut microbiota in health and disease. Physiol. Rev.90(3), 859–904 (2010).
  • Zhou L , ZhangM, WangYet al. Faecalibacterium prausnitzii produces butyrate to maintain Th17/Treg balance and to ameliorate colorectal colitis by inhibiting histone deacetylase 1. Inflamm. Bowel Dis.24(9), 1926–1940 (2018).
  • Wu S-E , Hashimoto-HillS, WooVet al. Microbiota-derived metabolite promotes HDAC3 activity in the gut. Nature586(7827), 108–112 (2020).
  • Luu M , PautzS, KohlVet al. The short-chain fatty acid pentanoate suppresses autoimmunity by modulating the metabolic-epigenetic crosstalk in lymphocytes. Nat. Commun.10(1), 760 (2019).
  • Furusawa Y , ObataY, FukudaSet al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature504(7480), 446–450 (2013).
  • Beier UH , WangL, HanR, AkimovaT, LiuY, HancockWW. Histone deacetylases 6 and 9 and sirtuin-1 control Foxp3+ regulatory T cell function through shared and isoform-specific mechanisms. Sci. Signal.5(229), ra45 (2012).
  • Wang L , LiuY, HanRet al. FOXP3+ regulatory T cell development and function require histone/protein deacetylase 3. J. Clin. Invest.125(3), 1111–1123 (2015).
  • Kim M , QieY, ParkJ, KimCH. Gut microbial metabolites fuel host antibody responses. Cell Host Microbe20(2), 202–214 (2016).
  • Sanchez HN , MoroneyJB, GanHet al. B cell-intrinsic epigenetic modulation of antibody responses by dietary fiber-derived short-chain fatty acids. Nat. Commun.11(1), 60 (2020).
  • Chen Y-C , ChuangC-H, MiaoZ-Fet al. Gut microbiota composition in chemotherapy and targeted therapy of patients with metastatic colorectal cancer. Front. Oncol.12, 955313 (2022).
  • Sanders ME , MerensteinDJ, ReidG, GibsonGR, RastallRA. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat. Rev. Gastroenterol. Hepatol.16(10), 605–616 (2019).
  • Ting NL-N , LauHC-H, YuJ. Cancer pharmacomicrobiomics: targeting microbiota to optimise cancer therapy outcomes. Gut71(7), 1412–1425 (2022).
  • Holscher HD . Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes8(2), 172–184 (2017).
  • Guarino MPL , AltomareA, EmerenzianiSet al. Mechanisms of action of prebiotics and their effects on gastro-intestinal disorders in adults. Nutrients12(4), 1037 (2020).
  • Hill C , GuarnerF, ReidGet al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol.11(8), 506–514 (2014).
  • Gopalakrishnan V , SpencerCN, NeziLet al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science359(6371), 97–103 (2018).
  • Zaharuddin L , MokhtarNM, MuhammadNawawi KN, RajaAli RA. A randomized double-blind placebo-controlled trial of probiotics in post-surgical colorectal cancer. BMC Gastroenterol.19(1), 131 (2019).
  • Ghanavati R , AsadollahiP, ShapourabadiMB, RazaviS, TalebiM, RohaniM. Inhibitory effects of lactobacilli cocktail on HT-29 colon carcinoma cells growth and modulation of the Notch and Wnt/β-catenin signaling pathways. Microb. Pathog.139, 103829 (2020).
  • Zhang Q , ZhaoQ, LiTet al. Lactobacillus plantarum-derived indole-3-lactic acid ameliorates colorectal tumorigenesis via epigenetic regulation of CD8(+) T cell immunity. Cell Metab.35(6), 943–960 (2023).
  • Lee HA , KimH, LeeK-W, ParkK-Y. Dead nano-sized Lactobacillus plantarum inhibits azoxymethane/dextran sulfate sodium-induced colon cancer in Balb/c mice. J. Med. Food18(12), 1400–1405 (2015).
  • Sivan A , CorralesL, HubertNet al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science350(6264), 1084–1089 (2015).
  • Vétizou M , PittJM, DaillèreRet al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science350(6264), 1079–1084 (2015).
  • Tukenmez U , AktasB, AslimB, YavuzS. The relationship between the structural characteristics of lactobacilli-EPS and its ability to induce apoptosis in colon cancer cells in vitro. Sci. Rep.9(1), 8268 (2019).
  • Halkjær SI , LoB, ColdFet al. Fecal microbiota transplantation for the treatment of irritable bowel syndrome: a systematic review and meta-analysis. World J. Gastroenterol.29(20), 3185–3202 (2023).
  • Blanchaert C , StrubbeB, PeetersH. Fecal microbiota transplantation in ulcerative colitis. Acta Gastroenterol. Belg.82(4), 519–528 (2019).
  • Routy B , LeChatelier E, DerosaLet al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science359(6371), 91–97 (2018).
  • Viaud S , SaccheriF, MignotGet al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science342(6161), 971–976 (2013).
  • Xu H , CaoC, RenYet al. Antitumor effects of fecal microbiota transplantation: implications for microbiome modulation in cancer treatment. Front. Immunol.13, 949490 (2022).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.