Impact of the Exposome on the Epigenome in Inflammatory Bowel Disease Patients and Animal Models
Abstract
:1. Introduction
2. Epigenetics in IBD
3. Methods
4. Results
4.1. Parental Exposition
4.2. Microbiota
Germ | Activity | Epigenetic Mechanism | Tissue/Cells | Mechanism | Model | Author |
---|---|---|---|---|---|---|
Commensal bacteria | ||||||
Commensal bacteria | Anti-inflammatory activity | miR-10a | DCs | Negatively regulates host miR-10a expression, which contribute to the intestinal homeostasis maintenance by targeting IL-12/IL-23p40 expression | C57BL/6 (B6) mice | Xue X, et al. (2011) [125] |
Commensal flora | Proinflammatory activity | miR-107 | DCs and macrophages | Downregulates miR-107 expression, known to represses the expression of IL-23p19, thereby favouring IL-23 expression | IECs, lamina propria CD11c+ myeloid cells including dendritic cells and macrophages, and T cells; DSS-induced colitis in mice | Xue X, et al. (2014) [126] |
Commensal bacteria | Anti-inflammatory activity | miR-10a | DCs | Inhibits human DCs miR-10a expression, which downregulates mucosal inflammatory response through inhibition of IL-12/IL-23p40 and NOD2 expression, and blockade of Th1/Th17 cell immune responses | Human monocyte-derived dendritic cells | Wu W, et al. (2015) [127] |
Commensal microbiome-dependent (Bacteroides acidifaciens and Lactobacillus johnsonii | Anti-inflammatory activity | miR-21-5p | IECs | Commensal microbiome-dependent miR-21-5p expression in IECs regulates intestinal epithelial permeability via ADP Ribosylation Factor 4 (ARF4) | HT-29 and Caco-2 cells | Nakata K., et al. (2017) [128] |
Cluster(s) | ||||||
↓ of Bacteroidetes and ↑ of protective Firmicutes and Clostridia | Anti-inflammatory activity | miR-21 | Colonic mucosae | Leads to miR-21 reduction, known to influence the pathogenesis of intestinal inflammation by causing propagation of a disrupted gut microbiota | WT and miR-21−/− mice | Johnston DGW, et al. (2018) [129] |
Cluster enriched in Bacteroides fragilis | - | DNA methylation | Intestinal mucosa | Induces 33 and 19 significantly hyper-methylated or hypomethylated sites, including hyper-methylated signals in the gene body of Notch Receptor 4 (NOTCH4) | 50 CD; 80 UC; 31 controls | Ryan FJ, et al. (2020) [130] |
Cluster enriched in Escherichia/Shigella/Klebsiella and Ruminococcus gnavus | Proinflammatory activity | DNA methylation | Intestinal mucosa | Larger number of differentially methylated CpG sites (131 hyper- and 475 hypomethylated), including hypomethylation in CCDC88B (recently correlated with risk of CD) and Transporter 2 (TAP2), involved in genetic heterogeneity of CD | ||
Cluster enriched in B. vulgatus | - | DNA methylation | Intestinal mucosa | Induces 23 hyper- and 18 hypomethylated sites, significant hyper-methylation was observed in the gene body of DNA Damage Regulated Autophagy Modulator 1 (DRAM1) | ||
Specific germ | ||||||
Adherent-invasive Escherichia coli (AIEC) | Proinflammatory activity | miR-30c and miR-130a | IECs | Upregulates levels of miR-30c and miR-130a in IECs (by activating NF-κB), reducing the levels of ATG5 and ATG16L1 and inhibiting autophagy, leading to increased numbers of intracellular AIEC and an increased inflammatory response | Cultured IECs and mouse enterocytes | Nguyen HT, et al. (2014) [115] |
AIEC | Proinflammatory activity | let-7b | IECs | Instigates excessive mucosal immune response against gut microbiota via miR let-7b/TLR4 signaling pathway | WT and IL-10 KO mice; T84 cells | Guo Z, et al. (2018) [117] |
AIEC | Proinflammatory activity | miR-30c and miR-130a | IECs | AIEC-infected IECs secretes exosomes that can transfer specific miRs (miR-30c and miR-130a) to recipient IECs, inhibiting autophagy-mediated clearance of intracellular AIEC | T84 cells | Larabi A, et al. (2020) [116] |
Mycobacterium avium subspecies paratuberculosis (MAP) | Proinflammatory activity | miR-21 | Macrophages | MAP upregulates miR-21 in macrophages, a change that results in diminished macrophages clearance ability and favours pathogens survival within the cells | THP-1 cells | Mostoufi-Afshar S, et al. (2018) [119] |
Lactobacillus rhamnosus GG | Anti-inflammatory activity | miR-146a and miR-155 | DCs | Induces a significant downregulation of miR-146a expression, a negative regulator of immune response, and upupregulation of on miR-155 | Cultured DCs | Giahi L., et al. (2012) |
Lactobacillus acidophilus | Anti-inflammatory activity | miRs | Colonic mucosae | L. acidophilus induce miRs expression | DSS-induced colitis in mice | Kim WK, et al. (2021) [131] |
Faecalibacterium prausnitzii | Anti-inflammatory activity | HDAC1 inhibition | T cells | Inhibits HDAC1, promotes Foxp3 and blocks the IL-6/STAT3/IL-17 downstream pathway contributing to the maintain of Th17/Treg balance | IBD patients (n = 9) and healthy control (n = 6); DSS-induced colitis in mice | Zhou L, et al. (2018) [132] |
Faecalibacterium prausnitzii | Anti-inflammatory activity | HDAC3 inhibition | T cells | Produces butyrate to decrease Th17 differentiation and attenuate colitis through inhibiting HDAC3 and c-Myc-related metabolism in T cells | IBD patients; TNBS-induced colitis in mice | Zhang M, et al. (2019) [133] |
Trichinella spiralis | Anti-inflammatory activity | miRs | T cells | Extra-vesicles-derived miR are involved in the regulation of the host immune response, including inflammation, including increase of Th2 and Treg cells | TNBS-induced colitis in mice | Yang Y, et al. (2020) [134] |
Enterotoxigenic Bacteroides fragilis (ETBF) | Proinflammatory activity | miR-149-3p | T cells | Downregulates miR-149-3p, which play a role in modulation of T-helper type 17 cell differentiation (with increased number of T-helper type 17 cell contributing to intestinal inflammation) | ETBF cells | Cao Y, et al. (2021) [135] |
Bacterial component | ||||||
Roseburia intestinalis-derived flagellin | Anti-inflammatory activity | lncRNA | IECs | Flagellin induces p38-stat1 activation, activated HIF1A-AS2 promotor, induced HIF1A-AS2 (a lncRNA) expression in gut epithelium in a dose- and time-dependent manner. HIF1A-AS2 inactivates NF-κB/Jnk pathway and thus inhibits inflammatory responses | DSS/Flagellin-challenged mice; Caco-2 cells | Quan Y, et al. (2018) [124] |
Roseburia intestinalis-derived flagellin | Anti-inflammatory activity | miR-223-3p | Macrophages | Flagellin inhibited activation of the NLRP3 inflammasome and pyroptosis via miR-223-3p/NLRP3 signaling in macrophages | DSS-induced colitis model in C57Bl/6 mice and the LPS/ATP-induced THP-1 macrophages | Wu X, et al. (2020) [123] |
LPS | Proinflammatory activity | H3K4me1, H3K4me3, and H3K27ac histone | Macrophages | Increases H3K4me1, H3K4me3, and H3K27ac histone marks, particularly in genes associated with an inflammatory response such as IL-12a and IL-18 | IL-10-deficient (Il10(−/−)) mice | Simon JM, et al. (2016) [136] |
LPS and flagellin | Anti-inflammatory activity | miR-146 | IECs | Stimulate miR-146a overexpression in IECs, induces immune tolerance, inhibiting cytokine production (MCP-1 and GROα/IL-8) | TNBS and DSS-induced colitis in mice | Anzola A, et al. (2018) [137] |
LPS | Proinflammatory activity | lncRNA H19 | IECs | Increases levels of H19 lncRNA in epithelial cells in the intestine. H19 lncRNA bound to p53 and miR (miR-34a and let-7) that inhibit cell proliferation (alters regeneration of the epithelium) | Intestinal tissues of UC patients and mice | Geng H, et al. (2018) [138] |
LPS | Proinflammatory activity | miR-19b | IECs | LPS significantly induces cell inflammatory injury, downregulated miR-19b expression and activates NF-κB and PI3K/AKT pathway | Caco2 cells | Qiao CX, et al. (2018) [120] |
LPS | Proinflammatory activity | lncRNA | Monocytes/macrophages | LPS promotes a downregulation of the lncRNA growth arrest-specific transcript 5 (GAS5), could mediate tissue damage by modulating the expression of matrix metalloproteinases | IBD patients (n = 25) | Lucafò M, et al. (2019) [139] |
LPS | Proinflammatory activity | miR-215 | Fibroblasts | LPS upregulates the expression of miR-215, increases oxidative stress in LPS-treated intestinal fibroblast by downregulating GDF11 (Growth differentiation factor 11) expression and activating the TLR4/NF-κB and JNK/p38 signaling pathways | CCD-18Co cells | Sun B, et al. (2020) [122] |
LPS | Proinflammatory activity | miR-506 and DNMT1 modification | IECs | LPS inhibits miR-506, leading to reduced expression of anion exchange protein 2 and inositol-1,4,5-trisphosphate-receptor but was accompanied by a substantial increase in DNMT1 and SPHK1 (sphingosine kinase 1) expression. The enhanced levels of kinase SPHK1 resulte in upregulation of bioactive sphingosine-1-phosphate (S1P) which led to further activation of S1P-dependent signaling pathways. The net effect of these responses is severe inflammation | Patients with PSC, PSC with concurrent UC (PSC + UC), UC alone, and healthy controls (n = 10 each); Caco2 cells | Kempinska-Podhorodecka A, et al. (2021) [140] |
LPS | Proinflammatory activity | miR-497 | Macrophages | Reduces miR-497, promotes the activation of NF-κB pathway and the release of cytokines | IBD patients, mice with colitis and LPS-treated RAW264.7 cells | Zhang M, et al. (2021) [121] |
4.3. Gut Microbiota-Derived Metabolites
4.4. Diet
Food | Activity | Epigenetic Mechanism | Tissue/Cells | Mechanism | Model | Author |
---|---|---|---|---|---|---|
Diet | ||||||
Western diet | Proinflammatory activity | miR-143, miR-145A, miR-148a, miR-152 | IECs | Leads to a decrease in miR-143/145a, miR-148a and miR-152 in colonocytes with a consequent increase in ADAM17 expression protein (these miRs regulating ADAM17) and aggravates colitis. | DSS-induced colitis in mice | Dougherty U, et al. (2021) [164] |
High fat diet | Proinflammatory activity | miR-155 | Visceral adipocytes | High fat diet changes the miR profile (among which miR-155) of the visceral adipose exosomes, switching the exosomes from anti-inflammatory to a proinflammatory phenotype. | Macrophages | Wei M, et al. (2020) [193] |
High fat diet rich in n-6 linoleic acid | Proinflammatory activity | DNA methylation | Colonic mucosae | Epigenetically modifies farnesoid-X-receptor (FXR), leading to the activation of downstream factors that participate in bile acid homeostasis and epigenetically activates prostaglandin-endoperoxide synthase-2 (Ptsg-2) coupled accumulation of c-JUN and proliferative cyclin D1(Ccnd1) and increase the risk of inflammation | C57BL/6J mice; Human colonic foetal cells | Romagnolo DF, et al. (2019) [194] |
Methyl-deficient diet | Proinflammatory activity | Sirtuin 1 | IECs | Reduces sirtuin 1 (SIRT1) expression level and promotes greater acetylation of (heat shock factor protein 1) HSF1, in relation with a dramatic decrease of chaperones (binding immunoglobulin protein (BIP), heat shock protein (HSP)27 and HSP90) | DSS-induced colitis in mice; Caco-2 cells | Melhem H, et al. (2016) [165] |
Low-methyl diet | Proinflammatory activity | DNA methylation | IECs | Low-methyl diet-dependent HRE demethylation led to abnormal gut expression of CEACAM6 (carcinoembryonic antigen-related cell adhesion molecule 6), favouring AIEC colonisation and subsequent inflammation | Transgenic mice; Caco-2, T-84 and sh-HIF1-α-T-84 cells | Denizot J, et al. (2015) [166] |
Methyl-donnor supplemented diet (folate, B12 vitamin) | Anti-inflammatory activity | DNA methylation | IECs | Methyl-donor supplemented diet contributes to hypermethylation of CEACAM6 promoter in IECs, associated with a significant decrease in CEACAM6 expression contributing to less adherence of AIEC bacteria to the enterocytes | CEABAC10 mice | Gimier E, et al. (2020) [195] |
Isolated food | ||||||
Cow’s milk (commercial) | Anti-inflammatory activity | miR-21, miR-29b and miR-125b | Colonic mucosae | Extracellular vesicles (EVs) concentrated from commercial cow’s milk downregulates miR-21, miR-29b and miR-125b. MiR-125b was associated with a higher expression of the NF-κB inhibitor TNFAIP3 (A20) | DSS-induced colitis in mice | Benmoussa A, et al. (2019) [178] |
Human milk derived exosomes | Anti-inflammatory activity | miR-320, miR-375, and Let-7 and DNMT1 and DNMT3 | Colonic mucosae | MiR highly express in milk, such as miR-320, 375, and Let-7, were found to be more abundant in the colon of milk derived exosomes-treated mice compared with untreated mice. These miR downregulate their target genes, mainly DNA methyltransferase 1 (DNMT1) and DNMT3 | DSS-induced colitis in mice; PBMC | Reif S, et al. (2020) [179] |
Dietary depletion of milk exosomes and their microRNA cargos | Proinflammatory activity | miR-200a-3p | Cecum mucosae | Elicits a depletion of miR-200a-3p and elevated intestinal inflammation and chemokine (C-X-C Motif) ligand 9 expression | Mdr1a−/− mice | Wu D, et al. (2019) [180] |
Saccharin sodium, Stevioside, and Sucralose (three common sweeteners) | Anti-inflammatory activity | miR-15b | IECs | Upregulate the expression of E-cadherin through the miR-15b/RECK/MMP-9 axis to improve intestinal barrier integrity. Saccharin exerts the most pronounced effect, followed by Stevioside and Sucralose | DSS-induced colitis in mice | Zhang X, et al. (2022) [181] |
Galacto-oligosaccharides (GOS) | Anti-inflammatory activity | miR-19 | IECs | GOS increases of cell viability, the decrease of apoptosis, as well as the suppressed release of TNF-α, IFN-γ and IL-1β by upregulating miR-19b | Human colon epithelial FHC cells; Helicobacter hepaticus induced colitis in rats | Sun J, et al. (2019) [182] |
Cinnamaldehyde (a major active compound from cinnamon) | Anti-inflammatory activity | miR-21 and miR-155 | Macrophages | Cinnamaldehyde inhibits NLRP3 inflammasome activation as well as miR-21 and miR-155 level in colon tissues and macrophage. The decrease in miR-21 and miR-155 suppresses levels of IL-1β and IL-6; | DSS-induced colitis in mice; macrophage cell line RAW264.7 and human monocytes U937 | Qu S, et al. (2018) [185] |
Cinnamaldehyde | Anti-inflammatory activity | lncRNAs H19 | T cells | Cinnamaldehyde inhibits Th17 cell differentiation by regulating the expression of lncRNA H19 | DSS-induced colitis in mice and naïve CD4+ T cells | Qu SL, et al. (2021) [101] |
Limonin (a triterpenoid extracted from citrus) | Anti-inflammatory activity | miR-124 | IECs | Downregulates p-STAT3/miR-214 signaling pathway and represses the productions of proinflammatory cytokines (such as TNF-α and IL-6) | DSS-induced colitis in mice; cultured normal colonic epithelial cells | Liu S, et al. (2019) [186] |
Edible ginger | Anti-inflammatory activity | Contained around 125 miRNAs | IECs | Increases the survival and proliferation of IECs, reduces the proinflammatory cytokines (such as TNF-α, IL-6 and IL-1β), and increases the anti-inflammatory cytokines (including IL-10 and IL-22) in colitis | DSS-induced colitis in mice | Zhang M, et al. (2016) [187] |
Ginsenoside Rh2 (active ingredient of ginseng) | Anti-inflammatory activity | miR-124 | IECs | Inhibits IL-6-induced STAT3 phosphorylation and miR-214 expression (which is an inflammatory effector molecule acting through NF-κB-IL6 pathway) | DSS-induced colitis in mice; cultured normal colonic epithelial cells | Chen X, et al. (2021) [188] |
Black raspberries (BRBs) | Anti-inflammatory activity | Demethylation the promoter of dkk3; correction of promoter hypermethylation of suppressor genes | Colonic mucosae | BRBs exert their anti-inflammatory effects is through decreasing NF-κB p65 expression leading to decrease of DNMT3B expression (but also histone deacetylases 1 and 2 (HDAC1 and HDAC2) and methyl-binding domain 2 or MBD2), which in turn reverse aberrant DNA methylation of tumor suppressor genes, e.g., dkk2, dkk3, in the Wnt pathway, resulting in their enhanced mRNA expression locally in colon and systematically in spleen and bone marrow and thus in decreased translocation of β-catenin to the nucleus prohibiting the activation of the pathway | DSS-induced colitis in mice; splenocytes and bone marrow cells | Wang LS, et al. (2013) [189] |
Black raspberries | Anti-inflammatory activity | Demethylation | Colonic mucosae | BRBs decreas the methylation of wif1, sox17, and qki gene promoters and thus increase their mRNA expression (contributing to Wnt signaling) | Interleukin-10 knockout mice | Wang LS, et al. (2013) [190] |
Mastiha | Anti-inflammatory activity | miR-155 | T cells | Plays a role in circulating levels of miR-155, a critical player in T helper-17 (Th17) differentiation and function | UC patients (n = 35) | Amerikanou C, et al. (2021) [196] |
Isoliquiritigenin | Anti-inflammatory activity | HDACs inhibition | IECs | Suppresses acetylated HMGB1 release via the induction of HDAC activity, which is one of the critical mediators of inflammation, which is actively secreted from inflammatory cytokine-stimulated immune or non-immune cells | HT-29 cells | Chi JH, et al. (2017) [197] |
Chronic ethanol exposure | Proinflammatory activity | miR-122a | IECs | Increases the intestinal miR-122a expression, which decreased occludin (OCLN) expression leading to increased intestinal permeability | HT-29 cells | Chen Y, et al. (2013) [191] |
Chronic alcohol feeding (but not acute alcohol binge) | Proinflammatory activity | miR-155 | Intestinal tissue | Increases miR-155 in the small bowel, which is a modulator of cytokine and T-cell immune response in the gut, leading to intestinal TNFα, and NF-κB activation | WT-mice | Lippai D, et al. (2014) [192] |
Polyphenol | ||||||
Polyphenolic red wine extract | Anti-inflammatory activity | miR-126 | Fibroblasts | Polyphenolic red wine extract downregulates miR-126, leading to downregulation of NF-kB, ICAM-1, VCAM-1, and PECAM-1 | CCD-18Co myofibroblasts cells | Angel-Morales G, et al. (2012) [198] |
Polyphenolic extracts from cowpea (Vigna unguiculata) | Anti-inflammatory activity | miR-126 | Fibroblasts | Cowpea may exert their anti-inflammatory activities at least in part through induction of miR-126 that then downregulate VCAM-1 mRNA and protein expressions | CCD-18Co myofibroblasts cells | Ojwang LO, et al. (2015) [199] |
Mango (Mangifera indica L.) polyphenolics | Anti-inflammatory activity | miR-126 | Fibroblasts | Mango polyphenols attenuates inflammatory response by modulating the PI3K/AKT/mTOR pathway at least in part through upregulation of miR-126 expression | CCD-18Co cells; DSS-induced colitis in rats | Kim H, et al. (2017) [200] |
Baicalin (flavone) | Anti-inflammatory activity | miR-191a | IECs | Exerts a protective effect on IECs against TNF-α-induced injury, which is at least partly via inhibiting the expression of miR-191a, thus increasing ZO-1 expression | IEC-6 cells | Wang L, et al. (2017) [170] |
Pomegranate (Punica granatum L.) polyphenolics | Anti-inflammatory activity | miR-145 | Myofibroblasts | Pomegranate polyphenols attenuate colitis by modulating the miR-145/p70S6K/HIF1α axis | DSS-induced colitis in rats; CCD-18Co colon-myofibroblastic cells | Kim H, et al. (2017) [201] |
Alpinetin, a flavonoid compound extracted from the seeds of Alpinia katsumadai Hayata | Anti-inflammatory activity | miR-302 | T cells | Activates Aryl hydrocarbon receptor (AhR), promoting expression of miR-302, downregulating expression of DNA methyltransferase 1 (DNMT-1), reducing methylation level of Foxp3 promoter region, facilitating combination of CREB and promoter region of Foxp3, and upregulating the expression of Foxp3. Alpinetin ameliorates colitis in mice by recovering Th17/Treg balance. | DSS-induced colitis in mice | Lv Q, et al. (2018) [168] |
Fortunellin, a citrus flavonoid | Anti-inflammatory activity | miR-374a | IECs | Fortunellin targets miR-374a, which is a negative regulator of PTEN, known to induce cell apoptosis | TNBS-induced colitis in rats | Xiong Y, et al. (2018) [169] |
Quercetin (flavonoid) | Anti-inflammatory activity | miR-369-3p | DCs | Quercetin-induced miR-369-3p which reduce C/EBP-β, TNF-α, and IL-6 production | LPS-stimulated DCs | Galleggiante V, et al. (2019) [171] |
Resveratrol (a natural plant product) | Anti-inflammatory activity | miR-31, Let7a, miR-132 | T cells | Resveratrol decreases the expression of several miRs (miR-31, Let7a, miR-132) that targets cytokines and transcription factors involved in anti-inflammatory T cell responses (Foxp3 and TGF-β). MiR-31 regulates the expression of Foxp3 with increase of CD4+ Foxp3+ regulatory T cells (Tregs) | TNBS-induced colitis in mice | Alrafas HR, et al. (2020) [176] |
Resveratrol (an anti-oxidant) | Anti-inflammatory activity | HDACs inhibition | T cells | Inhibits HDACs, increases anti-inflammatory CD4+ FOXP3+ (Tregs) and CD4+ IL10+ cells, and decreases proinflammatory Th1 and Th17 cells | AOM and DSS-induced colitis in mice | Alrafas HR, et al. (2020) [175] |
Chlorogenic acid (found in the coffee) | Anti-inflammatory activity | miR-155 | Macrophages | Downregulates miR-155 expression, inactivates the NF-κB/NLRP3 inflammasome pathway in macrophages and prevent colitis | DSS-induced colitis in mice; LPS/ATP-induced RAW264.7 cells | Zeng J, et al. (2020) [177] |
Lonicerin (constituant of herb Lonicera japonica Thunb.) | Anti-inflammatory activity | H3K27me3 modification | Macrophages | Binds to enhancer of zeste homolog 2 (EZH2) histone methyltransferase, which mediate modification of H3K27me3 and promotes the expression of autophagy-related protein 5, which in turn leads to enhanced autophagy and accelerates autolysosome-mediated NLRP3 degradation | DSS-induced colitis in mice and isolated colonic macrophages and IECs; bone marrow-derived macrophages | Lv Q, et al. (2021) [174] |
Pristimerin (Pris), which is a natural triterpenoid compound extracted from the Celastraceae plant | Anti-inflammatory activity | miR-155 | Colonic mucosae | Pris may reduce DSS-induced colitis in mice by inhibiting the expression of miR-155 | Blood and colon tissue of IBD patients; DSS-induced colitis in mice | Tian M, et al. (2021) [202] |
Cardamonin is a naturally occurring chalcone (majorly from the Zingiberaceae family incluging a wide range of spices from India) | Anti-inflammatory activity | Modulation of miR expression | Macrophages | Cardamonin modulates miR expression, protects the mice from DSS-induced colitis, decreases the expression of iNOS, TNF-α, and IL-6, and inhibited NF-kB signaling which emphasizes the role of cardamonin as an anti-inflammatory molecule | RAW 264.7 Cells (monocyte/macrophage-like cells); DSS-induced colitis in mice | James S, et al. (2021) [172] |
Berberine | Anti-inflammatory activity | miR-103a-3p | IECs | Represses Wnt/β-catenin pathway activation via modulating the miR-103a-3p/Bromodomain-containing protein 4 axis, thereby refraining pyroptosis and reducing the intestinal mucosal barrier defect induced via colitis | DSS-induced colitis in mice; Caco-2 cells and human NCM460 cells | Zhao X, et al. (2022) [173] |
4.5. Smoking
4.6. Drugs
4.7. Vitamin D
4.8. Physical Activity
5. Limitations to the Analysis of the Exposome Impact on the Epigenome in IBD
6. Conclusions and Challenge for the Future
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
Abbreviations
References
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Metabolite | Activity | Epigenetic Mechanism | Tissue/Cells | Mechanism | Model | Author |
---|---|---|---|---|---|---|
SCFAs | ||||||
SCFAs | Anti-inflammatory activity | HDACs inhibition | T cells | Inhibits HDACs in T cells and increases the acetylation of p70 S6 kinase and phosphorylation rS6, regulating the mTOR pathway required for generation of Th17 (T helper type 17), Th1, and IL-10(+) T cells | C57BL/6 mice; CD4+ T cells isolated from the spleen and lymph nodes | Park J, et al. (2015) [154] |
SCFAs | Anti-inflammatory activity | HDACs inhibition | B cells | Upregulates regulatory B cells capable of producing IL-10 in a manner dependent on their HDAC inhibitory activity | DSS-induced colitis in mice | Zou F, et al. (2021) [155] |
SCFAs | Anti-inflammatory activity | miR-145 | IECs | Decreases the CEBPB expression, which could bind to the miR-145 promoter to inhibit its expression, thereby promoting the expression of DUSP6 (dual-specificity phosphatase 6) and thus prevents the development of intestinal inflammation | LPS-treated intestinal epithelial cells | Liu Q, et al. (2022) [156] |
Butyrate | ||||||
Butyrate | Anti-inflammatory activity | Histone acetylation | IECs | Butyrate, by inducing an increase in histone acetylation in the NOD2 promoter region, induces NOD2 upregulation, and impact the defence mechanism against the bacterial membrane component peptidoglycan by inducing IL-8 and GRO-alpha secretion | Caco-2 cell line | Leung CH, et al. (2009) [147] |
Butyrate | Anti-inflammatory activity | HDAC inhibition | Dendritic cells | Butyrate has a role of HDACi on the epigenetic modification of gene expression, inhibits IL-12 and upregulates subunit IL-23p19 | DSS-induced colitis in mice | Berndt BE, et al. (2012) [153] |
Butyrate | Anti-inflammatory activity | HDAC1 inhibition | T cells | Butyrate inhibits HDAC1 activity to induce Fas promoter hyperacetylation and Fas upregulation in T cells and promote Fas-mediated apoptosis of T cells to eliminate the source of inflammation | BALB/c mice | Zimmerman MA, et al. (2012) [157] |
Butyrate | Anti-inflammatory activity | HDAC inhibition | IECs | Butyrate may contribute to the restoration of the tight junction barrier in IBD by affecting the expression of claudin-2, occludin, cingulin, and zonula occludens proteins (ZO-1, ZO-2) via inhibition of histone deacetylase | DSS-induced colitis in mice | Plöger S, et al. (2012) [146] |
Butyrate | Anti-inflammatory activity | Histone H3 acetylation | T cells | Butyrate enhances histone H3 acetylation in the promoter and conserves non-coding sequence regions of the Foxp3 locus, regulating the differentiation of Treg cells, ameliorating colitis | Germ-free and CRB-associated mice; OT-II (Ly5.2) transgenic CD4+ T cells | Furusawa Y, et al. (2013) [144] |
Butyrate | Anti-inflammatory activity | HDAC inhibition | Macrophages | Butyrate reduces de production of proinflammatory mediators by macrophages including nitric oxide, IL-6, and IL-12, but did not affect levels of TNF-α or MCP-1 | DSS-induced colitis in mice | Chang PV, et al. (2014) [149] |
Butyrate | Anti-inflammatory activity | H3K9 acetylation | Macrophages | Butyrate activates STAT6-mediated transcription through H3K9 acetylation driving M2 macrophage polarization | DSS-induced colitis in mice | Ji J, et al. (2016) [150] |
Butyrate | Anti-inflammatory activity | Histone H3 acetylation | Macrophages | Oral supplementation with butyrate attenuates experimental murine colitis by blocking NF-κB signaling and reverses histone acetylation | DSS-induced colitis in mice, IL-10−/− mice and RAW264.7 cells | Lee C, et al. (2017) [158] |
Butyrate | Anti or proinflammatory activity depending on its concentration and immunological milieu | HDACs inhibition | T cells | Lower butyrate concentrations facilitates differentiation of Tregs in vitro and in vivo under steady-state conditions. In contrast, higher concentrations of butyrate induces expression of the transcription factor T-bet in all investigated T cell subsets resulting in IFN-γ-producing Tregs or conventional T cells. This effect was mediated by the inhibition of histone deacetylase activity | DSS-induced colitis in mice; CD4+ T cells | Kespohl M, et al. (2017) [159] |
Butyrate | Anti-inflammatory activity | HDAC3 inhibition | MonocyteMacrophage | Butyrate induces the monocyte to macrophage differentiation and promotes its antimicrobial activity and restricts bacterial translocation, through HDAC3 inhibition | Human monocytes isolated from leukocyte cones of healthy blood donors | Schulthess J, et al. (2019) [148] |
Butyrate | Anti-inflammatory activity | HDAC inhibition | T cells | Butyrate promotes Th1 cell development by promoting IFN-γ and T-bet expression and inhibits Th17 cell development by suppressing IL-17, Rorα, and Rorγt expression and upregulate IL-10 production in Th1 and Th17 | CBir1 transgenic T cells; Rag1−/− mice | Chen L, et al. (2019) [151] |
Butyrate | Anti-inflammatory activity | Increase of histone acetylation | IECs | Butyrate induces HSF2 (Heat-shock transcription factor 2) expression epigenetically via increasing histone acetylation levels at the promoter region, enhancing autophagy in IECs | UC (n = 50) and healthy (n = 30) patients; DSS-induced colitis in mice; HT-29 cells | Zhang F, et al. (2020) [160] |
Butyrate | Anti-inflammatory activity | HDAC inhibition | IECs | Butyrate induces SYNPO (Synaptopodin) in epithelial cell lines through mechanisms possibly involving histone deacetylase inhibition. SYNPO contributes by intestinal homeostasis by controlling intestinal permeability | Epithelial cell lines; DSS-induced colitis in mice | Wang RX, et al. (2020) [161] |
Butyrate | Anti-inflammatory activity | HDAC inhibition | Neutrophils | Butyrate significantly inhibits IBD neutrophils to produce proinflammatory cytokines, chemokines, and calprotectins through HDAC inhibition | Peripheral neutrophils isolated from IBD patients and healthy donors; DSS-induced colitis in mice | Li G, et al. (2021) [152] |
Propionate | Anti-inflammatory activity | HDAC1 inhibition | IECs | Propionate promotes intestinal epithelial cell migration by enhancing cell spreading and polarization, a function dependant of the inhibition of class I HDAC | Mouse small intestinal epithelial cells (MSIE) and human Caco-2 cells; DSS-induced colitis in mice | Bilotta AJ, et al. (2021) [142] |
Caprylic acid (C8) and nonanoic acid (C9) (medium chain fatty acids) | Anti-inflammatory activity | Acetylation of histone 3 lysine 9 (H3K9) | IECs | Reduces bacterial translocation, enhances antibacterial activity, and attenuates the activity of the classical histone deacetylase pathway to facilitate the acetylation of histone 3 lysine 9 (H3K9) at the promoters pBD-1 and pBD-2, remarkably increases the secretion of porcine β-defensins 1 (pBD-1) and pBD-2 | Porcine jejunal epithelial cell line-J2 | Wang J, et al. (2018) [162] |
Drug | Activity | Epigenetic Mechanism | Tissue/Cells | Mechanism | Model | Author |
---|---|---|---|---|---|---|
IBD medication | ||||||
Mesalamine | Anti-inflammatory activity | miR-206 | IECs and colonic tissues | Long-term treatment donw-regulates miR-206 which confer a protective effect in inducing and maintaining histologic remission | HT29 colon cells; UC patients (n = 10) | Minacapelli CD, et al. (2019) [258] |
5-ASA | Anti-inflammatory activity | miR-125b, miR-150, miR-155, miR-346 and miR-506 | IECs | 5-ASA suppressed the levels of miR-125b, miR-150, miR-155, miR-346 and miR-506 in IECs and inhibition of these miR were associated with significant inductions of their target genes such as vitamin D receptor (VDR), suppressor of cytokine signaling (SOCS1), Forkhead box O (FOXO3a) and DNA methyltransferase 1 (DNMT1) | Caco-2 cells | Adamowicz M, et al. (2021) [259] |
Infliximab | Anti-inflammatory activity | miR-10a | DCs | Anti-TNF mAb treatment significantly promote miR-10a expression, whereas it markedly inhibited NOD2 and IL-12/IL-23p40 in the inflamed mucosa | Human monocyte-derived dendritic cells (DC); IBD patients | Wu W, et al. (2015) [127] |
Infliximab | Anti-inflammatory activity | miR-301a | T cells | Decreases miR-301a expression in IBD CD4+ T cells by decreasing Th17 cell differentiation through upregulation of SNIP1 | Peripheral blood mononuclear cells (PBMC); inflamed mucosa of patients with IBD | He C, et al. (2016) [260] |
Infliximab | Anti-inflammatory activity | lnc-ITSN1-2 | T cells | Lnc-ITSN1-2 promotes IBD CD4+ T cell activation, proliferation, and Th1/Th17 cell differentiation by serving as a competing endogenous RNA for IL-23R via sponging miR-125a | Intestinal mucosa from IBD patients (n = 6) and healthy controls (n = 6) | Nie J, et al. (2020) [261] |
Infliximab | Anti-inflammatory activity | miR-30 family | IECs | Decreases circRNA_103765 expression, which act as a molecular sponge to adsorb the miR-30 family and impair the negative regulation of Delta-like ligand 4 (DLL4) and protect human IECs from TNF-α-induced apoptosis | IBD patients; PBMCs | Ye Y, et al. (2021) [262] |
Infliximab | Anti-inflammatory activity | miR-146a and miR-146b | Serum and intestinal mucosae | Decreases miR-146a and miR-146b levels in serum. miR-146a probably promotes colitis through TLR4/MyD88/NF-κB signaling pathway | Serum of 19 IBD patients | Batra SK, et al. (2020) [263] |
Infliximab (IFX) therapy and longer-term steroids (weeks) | Anti-inflammatory activity | miR-320a | Decreases miR-320a serum level. miR-320a could play a role in sensitization of the quiescent mucosa to environmental factors | Serum of 19 IBD patients | ||
Anti-TNF and glucocorticoids | Anti-inflammatory activity | let-7c | let-7c serum level decreases, thus reduces M2 macrophage polarization (anti-inflammatory) and promote M1 (proinflammatory) polarization | Serum of 19 IBD patients | ||
Anti-TNF | Anti-inflammatory activity | miR-10a | DCs | Blockade TNF with anti-TNF mAb markedly enhances miR10a expression in the intestinal mucosa. miR-10a could block intestinal inflammation and reduce the differentiation Th1 and Th17 | C57BL/6 (B6) mice | Xue X, et al. (2011) [125] |
Anti-TNF | Anti-inflammatory activity | miR-378a-3p, miR-378c | Colonic mucosae | Increases levels of miR-378a-3p and miR-378c. Over-expression of miR-378a-3p decreased the levels of an IL-33 target sequence β-gal-reporter gene | Active UC patients (n = 24); inactive UC (n = 10); controls (n = 6); HEK293 cells | Dubois-Camacho K, et al. (2019) [264] |
Enemas containing short chain fatty acids (SCFA) such as butyrate, propionate, and acetate | Anti-inflammatory activity | Histone acetylation | IECs | SCFAs increase histone acetylation states and inhibit the production of proinflammatory substances, such as IL-8, by the intestinal epithelium | Caco-2 cells | Huang N, et al. (1997) [288] |
N-(1-carbamoyl-2-phenylethyl) butyramide (FBA), a butyrate-releasing derivative | Anti-inflammatory activity | Histone deacetylase-9 and H3 histone acetylation | Colonic mucosae | FBA, similar to its parental compound sodium butyrate, inhibited histone deacetylase-9 and restored H3 histone acetylation, exerting an anti-inflammatory effect through NF-κB inhibition and the upregulation of PPARγ | DSS-induced colitis in mice | Simeoli R, et al. (2017) [289] |
Exclusive enteral nutrition (EEN) | Anti-inflammatory activity | hsa-miR-192-5p, hsa-miR-423-3p, hsa-miR-99a-5p, hsa-miR-124-3p, hsa-miR-301a-5p, hsa-miR-495-5p, and hsa-let-7b-5p | Intestinal mucosae | EEN induces mucosal miRNAs expression profile (altered expressions of hsa-miR-192-5p, hsa-miR-423-3p, hsa-miR-99a-5p, hsa-miR-124-3p, hsa-miR-301a-5p, hsa-miR-495-5p, and hsa-let-7b-5p) after EEN therapy was significantly changed compared with inflamed mucosa before treatment | CD patients (n = 30) | Guo Z, et al. (2016) [265] |
ABX464 | Anti-inflammatory activity | miR-124 | Immune cells | Upregulates miR-124 in human immune cells, which is a negative regulator of inflammation and was shown to target RNAs, such as STAT and TLR | Tazi J, et al. (2021) [290] | |
MSCs | Anti-inflammatory activity | miR-181a | IECs | MSC-derived exosomal miR-181a could alleviate colitis by promoting intestinal barrier function decreased (increasing level of Claudin-1, ZO-1, and IκB) | DSS-induced colitis in mice and induced human colonic epithelial cell (HCOEPIC) | Gu L, et al. (2021) [266] |
MSCs | Anti-inflammatory activity | H3K27me3 | T cells | Extracellular vesicles from MSCs could inhibit the differentiation of Th17 cells by regulating H3K27me3 | TNBS-induced colitis in mice | Chen Q, et al. (2020) [291] |
IFN-γ pretreated bone marrow mesenchymal stem cells | Anti-inflammatory activity | miR-125a and miR-125b | T cells | Increases the level of miR-125a and miR-125b of exosomes, which directly targeted on Stat3, to repress Th17 cell differentiation | DSS-induced colitis in mice | Yang R, et al. (2020) [267] |
Vascular endothelial growth factor-C-treated adipose-derived stem cells (ADSCs) | Anti-inflammatory activity | miR-132 | Lymphatic endothelial cells | VEGF-C-treated ADSCs have a higher level of miR-132, which promotes lymphangiogenic response by directly targeting Smad-7 and regulating TGF-β/Smad signaling | Lymphatic endothelial cells (LECs) | Wang X, et al. (2018) [292] |
Supplementation | ||||||
Iron | Proinflammatory activity | TET1 induction; NRF2, NQ01, GPX2 demethylation | IECs and intestinal mucosae | Chronic iron exposure leads to induction of TET1 expression leading to demethylation of NRF2 (nuclear factor erythroid 2-related factor 2) pathway targets (including NAD(P)H Quinone Dehydrogenase 1 (NQO1) and Glutathione peroxidase 2 (GPX2). NQO1 and GPX2 hypomethylation led to increased gene and protein expression, and could be a route by which cells overcome persistent and chronic oxidative stress | Caco-2 cells and wild-type C57BL/6 mice | Horniblow RD, et al. (2022) [293] |
Antibiotics | ||||||
Isotretinoin | Anti-inflammatory activity | miR | T cells | 3 miR overexpressed in naive T-cells and potentially downregulate 777 miR targets (cytoskeleton remodelling and the c-Jun N terminal kinase (JNK) signaling pathway) | Balb/c mice | Becker E, et al. (2016) [268] |
Metronidazole | Anti-inflammatory activity | miR | 5 miR were significantly lower in naive T-cells resulting in the prediction of 340 potentially upregulated miR targets associated with IL-2 activation and signaling, cytoskeleton remodelling and epithelial-to-mesenchymal-transition (EMT). | |||
Doxycycline | Anti-inflammatory activity | miR-144-3p | Overexpression of miR-144-3p that resulted in the prediction of 493 potentially downregulated miR targets involved in protein kinase A (PKA), protein kinase B and nuclear factor of activated T-cells (NFAT) signaling pathways | |||
Tetracyclines | Anti-inflammatory activity | miR-150, miR-155, miR-375 and miR-146 | Colonic tissues | Reduce miR-150 and miR-155 expression, upregulate miR-375 and miR-142 | DSS-induced colitis in mice and bone marrow-derived macrophages | Garrido-Mesa J, et al. (2018) [269] |
Antibiotics treatment | Anti-inflammatory activity | DNA demethylation | IECs | Suppresses aberrant DNA methylation of three marker CpG islands (Cbln4, Fosb, and Msx1) induced by chronic inflammation | AOM/DSS-induced colitis in mice | Hattori N, et al. (2019) [270] |
Probiotics | ||||||
Probiotic bacterium Escherichia coli Nissle 1917 (EcN) | Anti-inflammatory activity | miR-203, miR-483-3p, miR-595 | IECs | Increases miR-203, miR-483-3p, miR-595 targeting tight junction (TJ) proteins; these miRNAs are involved in the regulation of barrier function by modulating the expression of regulatory and structural components of tight junctional complexes. | T84 cells | Veltman K, et al. (2012) [271] |
Bifidobacterium longum | Anti-inflammatory activity | DNA demethylation | Peripheral blood mononuclear cells | B. Longum treatment significantly demethylates several CpG sites in Foxp3 promoter | TNBS-induced colitis in rat; spleen peripheral blood mononuclear cells (PBMC) cells was extracted | Zhang M, et al. (2017) [272] |
Lactobacillus fermentum and Lactobacillus salivarius | Anti-inflammatory activity | miR-155, miR-223, miR-150 and miR-143 | Colonic tissues | They increase the expression of miR-155 and miR-223, and miR-150 and miR-143 for L. fermentum, involved in the immune response (restoration of Treg cell population and the Th1/Th2 cytokine balance) and in the intestinal barrier function | C57BL/6J mice | Rodríguez-Nogales A, et al. (2017) [273] |
Saccharomyces boulardii | Anti-inflammatory activity | miR-155 and miR-223; miR-143 and miR-375 | Colonic tissuess | Increasing the expression of miR-155 and miR-223, whereas decreasing the expression miR-143 and miR-375 | DSS-induced colitis in mice | Rodríguez-Nogales A, et al. (2018) [274] |
Bifidobacterium bifidum ATCC 29521 | Anti-inflammatory activity | miR-150, miR-155, miR-223 | Colonic mucosae | Restorates miR-150, miR-155, miR-223, upregulates anti-inflammatory cytokines (IL-10, PPARγ, IL-6), tight junction proteins (such as ZO-1, MUC-2, Claudin-3, and E Cadherin-1) and downregulates inflammatory genes (TNF-α, IL-1β) | DSS-induced colitis in mice | Din AU, et al. (2020) [275] |
Lactobacillus casei LH23 probiotic | Anti-inflammatory activity | Histone H3K9 acetylation | Colonic tissues | Modulates the immune response and ameliorates colitis via suppressing JNK/p-38 signal pathways and enhancing histone H3K9 acetylation | DSS-induced colitis in mice; LPS-induced RAW264.7 cells | Liu M, et al. (2020) [294] |
Lactic Acid-Producing Probiotic Saccharomyces cerevisiae | Anti-inflammatory activity | Histone H3K9 acetylation and histone H3K18 lactylation | Macrophages | Promotes histone H3K9 acetylation and histone H3K18 lactylation and attenuates intestinal inflammation via suppressing macrophage pyroptosis | DSS-induced colitis in mice | Sun S, et al. (2021) [276] |
Other medication | ||||||
Telmisartan (angiotensin II type 1 receptor blocker and a peroxisome proliferator-activated receptor-receptor-γ agonist) | Anti-inflammatory activity | miR-155 | Mesenteric adipocytes | Restorates the mesenteric adipose tissue adipocyte morphology and the expression of adipokines by suppressing the neurotensin/miR-155 pathway | IL-10(−)/(−) mice; cultured mesenteric adipose tissue from Crohn’s disease patients | Li Y, et al. (2015) [295] |
Melatonine | Anti-inflammatory activity | Prevent DNA methylation | IECs | Prevents DNA demethylation, reduces NF-κB activation, decreases the levels of inflammatory mediators (including IL-6, IL-8, COX-2, and NO), and reduces increase in paracellular permeability, attenuating the inflammatory response | Caco-2 cells | Mannino G, et al. (2019) [296] |
Morphine | Proinflammatory activity | Let7c-5p | Macrophages, DCs | Opioid treatment can disrupt gut immune homeostasis by inhibiting packaging of miR into EVs secreted by intestinal crypt cells (with a decreased amount of Let7c-5p) | C57BL/6J mice; organoid culture | Zhang Y, et al. (2021) [297] |
Artesunate | Anti-inflammatory activity | miR-155 | Macrophages | Inhibits the expression of miR-155 to inhibit the NF-κB pathway | LPS-induced RAW264.7 cells; BALB/c mice model | Yang ZB, et al. (2021) [298] |
Valproic acid treatment | Anti-inflammatory activity | HDAC inhibition | Intestinal tissue | Inhibits HDAC activity and increases H3K27ac levels and reduced expression of IL6, IL10, IL1B, and IL23 | DSS-induced colitis in mice | Felice C, et al. (2021) [299] |
Tetrandrine | Anti-inflammatory activity | miR-429 | IECs | Tetrandrine can attenuate the intestinal epithelial barrier defects in colitis through promoting occludin expression via the AhR/miR-429 pathway | DSS-induced colitis in mice | Chu Y, et al. (2021) [300] |
Chinese medicine | ||||||
Sinomenine, a pure alkaloid isolated in Chinese medicine | Anti-inflammatory activity | miR-155 | Colonic tissues | Downregulates the levels of miR-155 and several related inflammatory cytokines | TNBS-induced colitis in mice | Yu Q, et al. (2013) [277] |
Tripterygium wilfordii Hook F (TWHF) | Anti-inflammatory activity | miR-155 | Ileocolonic anastomosis | Triptolide could suppress miR-155/SHIP-1 signaling pathway and attenuated expression of inflammatory cytokines after ileocaecal resection | IL-10(−/−) mice | Wu R, et al. (2013) [278] |
Herb-partitioned moxibustion (HPM) | Anti-inflammatory activity | miR-147 and miR-205 | Colonic tissues | Upregulates the expression of miR-147 and miR-205 and then further regulate some of their target genes, thereby indirectly inhibiting the inflammatory signal pathways mediated by TLR, NF-κB, and so forth and decreasing the production of downstream inflammatory cytokines such as TNF-α and IL-1β, so as to alleviate intestinal inflammation in CD | Experimental CD rat models | Wei K, et al. (2015) [280] |
Salvianolic acid B (Sal B) is isolated from the traditional Chinese medical herb Salvia miltiorrhiza | Anti-inflammatory activity | miR-1 | IECs | Sal B restores barrier function by miR-1 activation and subsequent myosin light chain kinase (MLCK) inactivation | TNBS-induced rat colitis model | Xiong Y, et al. (2016) [281] |
Herb-partitioned moxibustion (HPM) | Anti-inflammatory activity | miR-184 and miR-490-5p | Colonic tissue | HPM regulates miR-184 and miR-490-5p expression, act on the transcription of their target genes to regulate inflammatory signaling pathways, and attenuate inflammation and tissue injury in the colons of rats with DSS-induced UC | DSS-induced colitis in mice | Huang Y, et al. (2017) [282] |
Triptolide (TPL) | Anti-inflammatory activity | miR-16-1 | Ileocolonic anastomosis | TPL reduces miR-16-1 levels aggravating anastomotic inflammation and fibrosis | IL-10−/− mice | Hou HW, et al. (2017) [283] |
Norisoboldine (NOR), a natural aryl hydrocarbon receptor (AhR) | Anti-inflammatory activity | H3K9me3 modification | T cells | NOR promoted Treg differentiation and then alleviated the development of colitis by regulating AhR (aryl hydrocarbon receptor)/glycolysis axis and decreases NAD+ and SIRT1 (sirtuin 1), facilitates the ubiquitin-proteasomal degradation of SUV39H1, which is a major member of histone KMTs and catalyses the H3K9me3 modification, which is associated with transcription repression of Foxp3 | Lv Q, et al. (2018) [284] | |
Triptolide (TPL), the most potent bioactive substance in TWHF (Tripterygium wilfordii Hook F) extract | Anti-inflammatory activity | miR-16-1 | Fibroblasts | Inhibits migration and proliferation of fibroblasts from ileocolonic anastomosis of CD patients via regulating the miR-16-1/HSP70 pathway | Fibroblasts from strictured anastomosis tissue (SAT) samples and matched anastomosis-adjacent normal tissue (NT) samples of CD patients (n = 10) | Chen M, et al. (2019) [285] |
Polysaccharide RAMPtp from Atractylodis macrocephalae Koidz | Anti-inflammatory activity | lncRNA ITSN1-OT1 | IECs | Induces lncRNA ITSN1-OT1, which blocks the nuclear import of phosphorylated STAT2 and prevents the decrease of expression and structural destroy of tight junction proteins | DSS-induced colitis in mice | Zong X, et al. (2021) [286] |
Dendrobium officinale polysaccharide (DOP) | Anti-inflammatory activity | miR-433-3p | IECs, macrophages | DOP interfered with the secretion of small extracellular vesicles (DIEs) by IEC, with increased miR-433-3p expression. When delivered to macrophages, miR-433-3p targeted the MAPK8 gene, leading to inhibition of the MAPK signaling pathway and reduced production of inflammatory cytokines | IECs, macrophages | Liu H, et al. (2021) [287] |
Huangqin-Tang decoction (HQT) | Anti-inflammatory activity | miR-185-3p | IECs | HQT could upregulate miR-185-3p, thereby affecting the myosin light chain kinase (MLCK)/myosin light chain phosphorylation (p-MLC) pathway and leading to increased expression of occludin protein, which ultimately protected the intestinal epithelial barrier function | Balb/c mice | Changlin Z, et al. (2021) [279] |
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Vieujean, S.; Caron, B.; Haghnejad, V.; Jouzeau, J.-Y.; Netter, P.; Heba, A.-C.; Ndiaye, N.C.; Moulin, D.; Barreto, G.; Danese, S.; et al. Impact of the Exposome on the Epigenome in Inflammatory Bowel Disease Patients and Animal Models. Int. J. Mol. Sci. 2022, 23, 7611. https://doi.org/10.3390/ijms23147611
Vieujean S, Caron B, Haghnejad V, Jouzeau J-Y, Netter P, Heba A-C, Ndiaye NC, Moulin D, Barreto G, Danese S, et al. Impact of the Exposome on the Epigenome in Inflammatory Bowel Disease Patients and Animal Models. International Journal of Molecular Sciences. 2022; 23(14):7611. https://doi.org/10.3390/ijms23147611
Chicago/Turabian StyleVieujean, Sophie, Bénédicte Caron, Vincent Haghnejad, Jean-Yves Jouzeau, Patrick Netter, Anne-Charlotte Heba, Ndeye Coumba Ndiaye, David Moulin, Guillermo Barreto, Silvio Danese, and et al. 2022. "Impact of the Exposome on the Epigenome in Inflammatory Bowel Disease Patients and Animal Models" International Journal of Molecular Sciences 23, no. 14: 7611. https://doi.org/10.3390/ijms23147611