MicroRNA Determines the Fate of Intestinal Epithelial Cell Differentiation and Regulates Intestinal Diseases

Author(s): Sujuan Ding, Gang Liu, Hongmei Jiang*, Jun Fang*.

Journal Name: Current Protein & Peptide Science

Volume 20 , Issue 7 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

The rapid self-renewal of intestinal epithelial cells enhances intestinal function, promotes the nutritional needs of animals and strengthens intestinal barrier function to resist the invasion of foreign pathogens. MicroRNAs (miRNAs) are a class of short-chain, non-coding RNAs that regulate stem cell proliferation and differentiation by down-regulating hundreds of conserved target genes after transcription via seed pairing to the 3' untranslated regions. Numerous studies have shown that miRNAs can improve intestinal function by participating in the proliferation and differentiation of different cell populations in the intestine. In addition, miRNAs also contribute to disease regulation and therefore not only play a vital role in the gastrointestinal disease management but also act as blood or tissue biomarkers of disease. As changes to the levels of miRNAs can change cell fates, miRNA-mediated gene regulation can be used to update therapeutic strategies and approaches to disease treatment.

Keywords: miRNA, intestinal stem cells, differentiation, cancer, inflammatory bowel disease, mucosal inflammation.

[1]
Heath, J.P. Epithelial cell migration in the intestine. Cell Biol. Int., 1996, 20(2), 139-146.
[2]
Potten, C.S. Kinetics and possible regulation of crypt cell populations under normal and stress conditions. Bull. Cancer, 1975, 62(4), 419-430.
[3]
Biswas, S.; Davis, H.; Irshad, S.; Sandberg, T.; Worthley, D.; Leedham, S. Microenvironmental control of stem cell fate in intestinal homeostasis and disease. J. Pathol., 2015, 237(2), 135-145.
[4]
Barker, N. Adult intestinal stem cells: Critical drivers of epithelial homeostasis and regeneration. Nat. Rev. Mol. Cell Biol., 2014, 15(1), 19.
[5]
Van Der Flier, L.G.; Clevers, H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol., 2009, 71, 241-260.
[6]
Gong, X.; Chao, R.; Wang, P.; Huang, X.; Zhang, J.; Zhu, X.; Zhang, Y.; Yang, X.; Hou, C.; Ji, X.; Shi, T.; Wang, Y. Interplay of transcription factors and microRNAs during embryonic hematopoiesis. Sci. China Life Sci., 2017, 60(2), 168-177.
[7]
Lai, Y.; Gallo, R.L. AMPed up immunity: How antimicrobial peptides have multiple roles in immune defense. Trends Immunol., 2009, 30(3), 131-141.
[8]
Keshav, S. Paneth cells: Leukocyte-like mediators of innate immunity in the intestine. J. Leukoc. Biol., 2006, 80(3), 500-508.
[9]
Muniz, L.R.; Knosp, C.; Yeretssian, G. Intestinal antimicrobial peptides during homeostasis, infection, and disease. Front. Immunol., 2012, 3, 310.
[10]
Shenoy, A.; Blelloch, R.H. Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat. Rev. Mol. Cell Biol., 2014, 15(9), 565.
[11]
Reinhart, B.J.; Weinstein, E.G.; Rhoades, M.W.; Bartel, B.; Bartel, D.P. MicroRNAs in plants. Genes Dev., 2002, 16(13), 1616-1626.
[12]
Wang, L.; Wang, J.W. Coding function for non-coding RNA in plants-insights from miRNA encoded peptide (miPEP). Sci. China Life Sci., 2015, 58(5), 503.
[13]
Polyak, K.; Weinberg, R.A. Transitions between epithelial and mesenchymal states: Acquisition of malignant and stem cell traits. Nat. Rev. Cancer, 2009, 9(4), 265.
[14]
Sandberg, R.; Neilson, J.R.; Sarma, A.; Sharp, P.A.; Burge, C.B. Proliferating cells express mRNAs with shortened 3'untranslated regions and fewer microRNA target sites. Science, 2008, 320(5883), 1643-1647.
[15]
Li, X.; Huang, C.; Xue, Y. Contribution of lipids in honeybee (Apis mellifera) royal jelly to health. J. Med. Food, 2013, 16(2), 96-102.
[16]
Gangaraju, V.K.; Lin, H. MicroRNAs: Key regulators of stem cells. Nat. Rev. Mol. Cell Biol., 2009, 10(2), 116-125.
[17]
Shenoy, A.; Blelloch, R.H. Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat. Rev. Mol. Cell Biol., 2014, 15(9), 565.
[18]
van der Flier, L.G.; Clevers, H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol., 2009, 71, 241-260.
[19]
Lg, V.D.F.; Clevers, H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol., 2009, 71(71), 241-260.
[20]
Chen, S.; Wang, M.; Yin, L.; Ren, W.; Bin, P.; Xia, Y.; Liu, G.; Yang, H.; Tan, B.; Yin, Y. Effects of dietary tryptophan supplementation in the acetic acid-induced colitis mouse model. Food Funct., 2018, 9(8), 4143-4152.
[21]
Van Es, J.H.; Sato, T.; Van De Wetering, M.; Lyubimova, A.; Nee, A.N.Y.; Gregorieff, A.; Sasaki, N.; Zeinstra, L.; Van Den Born, M.; Korving, J. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol., 2012, 14(10), 1099.
[22]
Gerbe, F.; van Es, J.H.; Makrini, L.; Brulin, B.; Mellitzer, G.; Robine, S.; Romagnolo, B.; Shroyer, N.F.; Bourgaux, J.F.; Pignodel, C. Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J. Cell Biol., 2011, 192(5), 767-780.
[23]
Herranz, H.; Cohen, S.M. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev., 2010, 24(13), 1339-1344.
[24]
Ebert, M.S.; Sharp, P.A. Roles for microRNAs in conferring robustness to biological processes. Cell, 2012, 149(3), 515-524.
[25]
Hattangadi, S.M.; Wong, P.; Zhang, L.; Flygare, J.; Lodish, H.F. From stem cell to red cell: Regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood, 2011, 118(24), 6258-6268.
[26]
Shyh-Chang, N.; Daley, G.Q. Lin28: Primal regulator of growth and metabolism in stem cells. Cell Stem Cell, 2013, 12(4), 395-406.
[27]
Shcherbata, H.R.; Ward, E.J.; Fischer, K.A.; Yu, J.Y.; Reynolds, S.H.; Chen, C.H.; Xu, P.; Hay, B.A.; Ruohola-Baker, H. Stage-specific differences in the requirements for germline stem cell maintenance in the Drosophila ovary. Cell Stem Cell, 2007, 1(6), 698-709.
[28]
Koh, W.; Sheng, C.T.; Tan, B.; Lee, Q.Y.; Kuznetsov, V.; Kiang, L.S.; Tanavde, V. Analysis of deep sequencing microRNA expression profile from human embryonic stem cells derived mesenchymal stem cells reveals possible role of let-7 microRNA family in downstream targeting of hepatic nuclear factor 4 alpha. BMC Genomics, 2010, 11(1), S6.
[29]
Yu, Y.; Liao, L.; Shao, B.; Su, X.; Shuai, Y.; Wang, H.; Shang, F.; Zhou, Z.; Yang, D.; Jin, Y. Knockdown of microRNA let-7a improves the functionality of bone marrow-derived mesenchymal stem cells in immunotherapy. Mol. Ther., 2017, 25(2), 480-493.
[30]
Anokye-Danso, F.; Trivedi, C.M.; Juhr, D.; Gupta, M.; Cui, Z.; Tian, Y.; Zhang, Y.; Yang, W.; Gruber, P.J.; Epstein, J.A.; Morrisey, E.E. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell, 2011, 8(4), 376-388.
[31]
Miyoshi, N.; Ishii, H.; Nagano, H.; Haraguchi, N.; Dewi, D.L.; Kano, Y.; Nishikawa, S.; Tanemura, M.; Mimori, K.; Tanaka, F.; Saito, T.; Nishimura, J.; Takemasa, I.; Mizushima, T.; Ikeda, M.; Yamamoto, H.; Sekimoto, M.; Doki, Y.; Mori, M. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell, 2011, 8(6), 633-638.
[32]
Peck, B.C.; Sincavage, J.; Feinstein, S.; Mah, A.T.; Simmons, J.G.; Lund, P.K.; Sethupathy, P. miR-30 family controls proliferation and differentiation of intestinal epithelial cell models by directing a broad gene expression program that includes SOX9 and the ubiquitin ligase pathway. J. Biol. Chem., 2016, 291(31), 15975-15984.
[33]
Xia, Z.Q.; Ding, D.K.; Zhang, N.; Wang, J.X.; Yang, H.Y.; Zhang, D. MicroRNA-211 causes ganglion cell dysplasia in congenital intestinal atresia via down-regulation of glial-derived neurotrophic factor. Neurogastroenterol. Motil., 2016, 28(2), 186-195.
[34]
Dalmasso, G.; Nguyen, H.T.; Yan, Y.; Laroui, H.; Srinivasan, S.; Sitaraman, S.V.; Merlin, D. MicroRNAs determine human intestinal epithelial cell fate. Differentiation, 2010, 80(2-3), 147-154.
[35]
Chen, F.; Liu, H.; Wu, J.; Zhao, Y. miR-125a suppresses TrxR1 expression and is involved in H2O2-induced oxidative stress in endothelial cells. J. Immunol. Res., 2018, 20186140320
[36]
Hino, K.; Tsuchiya, K.; Fukao, T.; Kiga, K.; Okamoto, R.; Kanai, T.; Watanabe, M. Inducible expression of microRNA-194 is regulated by HNF-1alpha during intestinal epithelial cell differentiation. RNA, 2008, 14(7), 1433-1442.
[37]
Owen, R.L.; Jones, A.L. Epithelial cell specialization within human Peyer’s patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology, 1974, 66(2), 189-203.
[38]
Nakato, G.; Hase, K.; Sato, T.; Kimura, S.; Sakakibara, S.; Sugiyama, M.; Obata, Y.; Hanazato, M.; Iwanaga, T.; Ohno, H. Epithelium-intrinsic microRNAs contribute to mucosal immune homeostasis by promoting m-cell maturation. PLoS One, 2016, 11(3)e0150379
[39]
Ding, S.; Jiang, H.; Fang, J. Regulation of immune function by polyphenols. J. Immunol. Res., 2018, 20181264074
[40]
Liao, Y.; Lonnerdal, B. Beta-catenin/TCF4 transactivates miR-30e during intestinal cell differentiation. Cell. Mol. Life Sci., 2010, 67(17), 2969-2978.
[41]
Foronda, D.; Weng, R.; Verma, P.; Chen, Y.W.; Cohen, S.M. Coordination of insulin and Notch pathway activities by microRNA miR-305 mediates adaptive homeostasis in the intestinal stem cells of the Drosophila gut. Genes Dev., 2014, 28(21), 2421-2431.
[42]
Nguyen, H.T.T.; Dalmasso, G.; Yan, Y.; Laroui, H.; Dahan, S.; Mayer, L.; Sitaraman, S.V.; Merlin, D. MicroRNA-7 modulates CD98 expression during intestinal epithelial cell differentiation. J. Biol. Chem., 2010, 285(2), 1479-1489.
[43]
Chen, Y.; Xiao, Y.; Ge, W.; Zhou, K.; Wen, J.; Yan, W.; Wang, Y.; Wang, B.; Qu, C.; Wu, J.; Xu, L.; Cai, W. miR-200b inhibits TGF-β1-induced epithelial-mesenchymal transition and promotes growth of intestinal epithelial cells. Cell Death Dis., 2013, 4(3)e541
[44]
Dalmasso, G.; Nguyen, H.T.; Yan, Y.; Laroui, H.; Charania, M.A.; Obertone, T.S.; Sitaraman, S.V.; Merlin, D. MicroRNA-92b regulates expression of the oligopeptide transporter PepT1 in intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol., 2011, 300(1), G52-G59.
[45]
Hino, K.; Fukao, T.; Watanabe, M. Regulatory interaction of HNF1-alpha to microRNA-194 gene during intestinal epithelial cell differentiation. Nucleic Acids Symp. Ser. (Oxf), 2007, 51, 415-416.
[46]
Liu, Z.; Chen, X.; Wu, Q.; Song, J.; Wang, L.; Li, G. miR-125b inhibits goblet cell differentiation in allergic airway inflammation by targeting SPDEF. Eur. J. Pharmacol., 2016, 782, 14-20.
[47]
Shan, T.D.; Ouyang, H.; Yu, T.; Li, J.Y.; Huang, C.Z.; Yang, H.S.; Zhong, W.; Xia, Z.S.; Chen, Q.K. miRNA-30e regulates abnormal differentiation of small intestinal epithelial cells in diabetic mice by downregulating Dll4 expression. Cell Prolif., 2016, 49(1), 102-114.
[48]
Zhou, H.; Xiao, J.; Wu, N.; Liu, C.; Xu, J.; Liu, F.; Wu, L. MicroRNA-223 regulates the differentiation and function of intestinal dendritic cells and macrophages by targeting C/EBPbeta. Cell Rep., 2015, 13(6), 1149-1160.
[49]
McKenna, L.B.; Schug, J.; Vourekas, A.; McKenna, J.B.; Bramswig, N.C.; Friedman, J.R.; Kaestner, K.H. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology, 2010, 139(5), 1654-1664.
[50]
Rebane, A.; Akdis, C.A. MicroRNAs: Essential players in the regulation of inflammation. J. Allergy Clin. Immunol., 2013, 132(1), 15-26.
[51]
Lim, L.P.; Lau, N.C.; Garrett-Engele, P.; Grimson, A.; Schelter, J.M.; Castle, J.; Bartel, D.P.; Linsley, P.S.; Johnson, J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature, 2005, 433(7027), 769-773.
[52]
Belcheva, A. MicroRNAs at the epicenter of intestinal homeostasis. BioEssays, 2017, 39(3)1600200
[53]
Chinen, I.; Nakahama, T.; Kimura, A.; Nguyen, N.T.; Takemori, H.; Kumagai, A.; Kayama, H.; Takeda, K.; Lee, S.; Hanieh, H.; Ripley, B.; Millrine, D.; Dubey, P.K.; Nyati, K.K.; Fujii-Kuriyama, Y.; Chowdhury, K.; Kishimoto, T. The aryl hydrocarbon receptor/microRNA-212/132 axis in T cells regulates IL-10 production to maintain intestinal homeostasis. Int. Immunol., 2015, 27(8), 405-415.
[54]
Zhang, Y.; Viennois, E.; Zhang, M.; Xiao, B.; Han, M.K.; Walter, L.; Garg, P.; Merlin, D. PepT1 expression helps maintain intestinal homeostasis by mediating the differential expression of miRNAs along the crypt-villus axis. Sci. Rep., 2016, 6, 27119.
[55]
Kim, H.Y.; Kwon, H.Y.; Ha Thi, H.T.; Lee, H.J.; Kim, G.I.; Hahm, K.B.; Hong, S. MicroRNA-132 and microRNA-223 control positive feedback circuit by regulating FOXO3a in inflammatory bowel disease. J. Gastroenterol. Hepatol., 2016, 31(10), 1727-1735.
[56]
Wang, H.; Chao, K.; Ng, S.C.; Bai, A.H.; Yu, Q.; Yu, J.; Li, M.; Cui, Y.; Chen, M.; Hu, J.F.; Zhang, S. Pro-inflammatory miR-223 mediates the cross-talk between the IL23 pathway and the intestinal barrier in inflammatory bowel disease. Genome Biol., 2016, 17(1), 58.
[57]
Zahm, A.M.; Hand, N.J.; Tsoucas, D.M.; Le Guen, C.L.; Baldassano, R.N.; Friedman, J.R. Rectal microRNAs are perturbed in pediatric inflammatory bowel disease of the colon. J. Crohn’s Colitis, 2014, 8(9), 1108-1117.
[58]
Asaoka, T.; Sotolongo, B.; Island, E.R.; Tryphonopoulos, P.; Selvaggi, G.; Moon, J.; Tekin, A.; Amador, A.; Levi, D.M.; Garcia, J.; Smith, L.; Nishida, S.; Weppler, D.; Tzakis, A.G.; Ruiz, P. MicroRNA signature of intestinal acute cellular rejection in formalin-fixed paraffin-embedded mucosal biopsies. Am. J. Transplant., 2012, 12(2), 458-468.
[59]
Gutierrez-Camino, A.; Oosterom, N.; den Hoed, M.A.H.; Lopez-Lopez, E.; Martin-Guerrero, I.; Pluijm, S.M.F.; Pieters, R.; de Jonge, R.; Tissing, W.J.E.; Heil, S.G.; Garcia-Orad, A.; van den Heuvel-Eibrink, M.M. The miR-1206 microRNA variant is associated with methotrexate-induced oral mucositis in pediatric acute lymphoblastic leukemia. Pharmacogenet. Genomics, 2017, 27(8), 303-306.
[60]
He, C.; Shi, Y.; Wu, R.; Sun, M.; Fang, L.; Wu, W.; Liu, C.; Tang, M.; Li, Z.; Wang, P.; Cong, Y.; Liu, Z. miR-301a promotes intestinal mucosal inflammation through induction of IL-17A and TNF-alpha in IBD. Gut, 2016, 65(12), 1938-1950.
[61]
Zhao, Y.; Ma, T.; Chen, W.; Chen, Y.; Li, M.; Ren, L.; Chen, J.; Cao, R.; Feng, Y.; Zhang, H.; Shi, R. MicroRNA-124 promotes intestinal inflammation by targeting aryl hydrocarbon receptor in crohn’s disease. J. Crohn’s Colitis, 2016, 10(6), 703-712.
[62]
He, C.; Yu, T.; Shi, Y.; Ma, C.; Yang, W.; Fang, L.; Sun, M.; Wu, W.; Xiao, F.; Guo, F.; Chen, M.; Yang, H.; Qian, J.; Cong, Y.; Liu, Z. MicroRNA 301A promotes intestinal inflammation and colitis-associated cancer development by inhibiting BTG1. Gastroenterology, 2017, 152(6), 1434-1448.e15.
[63]
Jung, C.K.; Jung, S.H.; Yim, S.H.; Jung, J.H.; Choi, H.J.; Kang, W.K.; Park, S.W.; Oh, S.T.; Kim, J.G.; Lee, S.H.; Chung, Y.J. Predictive microRNAs for lymph node metastasis in endoscopically resectable submucosal colorectal cancer. Oncotarget, 2016, 7(22), 32902-32915.
[64]
Zekri, A.R.; Youssef, A.S.; Lotfy, M.M.; Gabr, R.; Ahmed, O.S.; Nassar, A.; Hussein, N.; Omran, D.; Medhat, E.; Eid, S.; Hussein, M.M.; Ismail, M.Y.; Alenzi, F.Q.; Bahnassy, A.A. Circulating serum miRNAs as diagnostic markers for colorectal cancer., PLoS One, . 201, 11(5), e0154130.
[65]
Xavier, R.J.; Podolsky, D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature, 2007, 448(7152), 427-434.
[66]
Cho, J.H. The genetics and immunopathogenesis of inflammatory bowel disease. Nat. Rev. Immunol., 2008, 8(6), 458-466.
[67]
Brain, O.; Owens, B.M.; Pichulik, T.; Allan, P.; Khatamzas, E.; Leslie, A.; Steevels, T.; Sharma, S.; Mayer, A.; Catuneanu, A.M. The intracellular sensor NOD2 induces microRNA-29 expression in human dendritic cells to limit IL-23 release. Immunity, 2013, 39(3), 521-536.
[68]
Wu, F.; Zikusoka, M.; Trindade, A.; Dassopoulos, T.; Harris, M.L.; Bayless, T.M.; Brant, S.R.; Chakravarti, S.; Kwon, J.H. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology, 2008, 135(5), 1624-1635.e24.
[69]
Neudecker, V.; Yuan, X.; Bowser, J.L.; Eltzschig, H.K. MicroRNAs in mucosal inflammation. J. Mol. Med. (Berl.), 2017, 95(9), 935-949.
[70]
Oertli, M.; Engler, D.B.; Kohler, E.; Koch, M.; Meyer, T.F.; Muller, A. MicroRNA-155 is essential for the T cell-mediated control of Helicobacter pylori infection and for the induction of chronic gastritis and colitis. J. Immunol., 2011, 187(7), 3578-3586.
[71]
Wu, W.; He, C.; Liu, C.; Cao, A.T.; Xue, X.; Evans-Marin, H.L.; Sun, M.; Fang, L.; Yao, S.; Pinchuk, I.V.; Powell, D.W.; Liu, Z.; Cong, Y. miR-10a inhibits dendritic cell activation and Th1/Th17 cell immune responses in IBD. Gut, 2015, 64(11), 1755-1764.
[72]
Yang, X.; He, Q.; Guo, Z.; Xiong, F.; Li, Y.; Pan, Y.; Gao, C.; Li, L.; He, C. MicroRNA-425 facilitates pathogenic Th17 cell differentiation by targeting forkhead box O1 (Foxo1) and is associated with inflammatory bowel disease. Biochem. Biophys. Res. Commun., 2018, 496(2), 352-358.
[73]
Xiao, B.; Liu, Z.; Li, B.S.; Tang, B.; Li, W.; Guo, G.; Shi, Y.; Wang, F.; Wu, Y.; Tong, W.D.; Guo, H.; Mao, X.H.; Zou, Q.M. Induction of microRNA-155 during Helicobacter pylori infection and its negative regulatory role in the inflammatory response. J. Infect. Dis., 2009, 200(6), 916-925.
[74]
Chen, Y.; Xiao, Y.; Ge, W.; Zhou, K.; Wen, J.; Yan, W.; Wang, Y.; Wang, B.; Qu, C.; Wu, J. miR-200b inhibits TGF-β1-induced epithelial-mesenchymal transition and promotes growth of intestinal epithelial cells. Cell Death Dis., 2013, 4(3)e541
[75]
Xiao, Y-T.; Wang, J.; Lu, W.; Cao, Y.; Cai, W. Downregulated expression of microRNA-124 in pediatric intestinal failure patients modulates macrophages activation by inhibiting STAT3 and AChE. Cell Death Dis., 2016, 7(12)e2521
[76]
Chen, T.; Xue, H.; Lin, R.; Huang, Z. MiR-34c and PlncRNA1 mediated the function of intestinal epithelial barrier by regulating tight junction proteins in inflammatory bowel disease. Biochem. Biophys. Res. Commun., 2017, 486(1), 6-13.
[77]
Maharshak, N.; Shenhar-Tsarfaty, S.; Aroyo, N.; Orpaz, N.; Guberman, I.; Canaani, J.; Halpern, Z.; Dotan, I.; Berliner, S.; Soreq, H. MicroRNA-132 modulates cholinergic signaling and inflammation in human inflammatory bowel disease. Inflamm. Bowel Dis., 2013, 19(7), 1346-1353.
[78]
Ghorpade, D.S.; Sinha, A.Y.; Holla, S.; Singh, V.; Balaji, K.N. NOD2-nitric oxide-responsive microRNA-146a activates Sonic hedgehog signaling to orchestrate inflammatory responses in murine model of inflammatory bowel disease. J. Biol. Chem., 2013, 288(46), 33037-33048.
[79]
Li, M.; Zhang, S.; Qiu, Y.; He, Y.; Chen, B.; Mao, R.; Cui, Y.; Zeng, Z.; Chen, M. Upregulation of miR-665 promotes apoptosis and colitis in inflammatory bowel disease by repressing the endoplasmic reticulum stress components XBP1 and ORMDL3. Cell Death Dis., 2017, 8(3)e2699
[80]
Olaru, A.V.; Yamanaka, S.; Vazquez, C.; Mori, Y.; Cheng, Y.; Abraham, J.M.; Bayless, T.M.; Harpaz, N.; Selaru, F.M.; Meltzer, S.J. MicroRNA-224 negatively regulates p21 expression during late neoplastic progression in inflammatory bowel disease. Inflamm. Bowel Dis., 2013, 19(3), 471-480.
[81]
Guo, J.; Sun, M.; Teng, X.; Xu, L. MicroRNA75p regulates the expression of TFF3 in inflammatory bowel disease. Mol. Med. Rep., 2017, 16(2), 1200-1206.
[82]
Artis, D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol., 2008, 8(6), 411.
[83]
Park, J.S.; Choi, J.W.; Jhun, J.; Kwon, J.Y.; Lee, B.I.; Yang, C.W.; Park, S.H.; Cho, M.L. Lactobacillus acidophilus improves intestinal inflammation in an acute colitis mouse model by regulation of Th17 and treg cell balance and fibrosis development. J. Med. Food, 2018, 21(3), 215-224.
[84]
Ashley, N. Regulation of intestinal cancer stem cells. Cancer Lett., 2013, 338(1), 120-126.
[85]
Azarbarzin, S.; Feizi, M.A.H.; Safaralizadeh, R.; Kazemzadeh, M.; Fateh, A. The value of miR-383, an intronic miRNA, as a diagnostic and prognostic biomarker in intestinal-type gastric cancer. Biochem. Genet., 2017, 55(3), 244-252.
[86]
Zeitels, L.R.; Acharya, A.; Shi, G.; Chivukula, D.; Chivukula, R.R.; Anandam, J.L.; Abdelnaby, A.A.; Balch, G.C.; Mansour, J.C.; Yopp, A.C.; Richardson, J.A.; Mendell, J.T. Tumor suppression by miR-26 overrides potential oncogenic activity in intestinal tumorigenesis. Genes Dev., 2014, 28(23), 2585-2590.
[87]
Nakaoka, T.; Saito, Y.; Shimamoto, Y.; Muramatsu, T.; Kimura, M.; Kanai, Y.; Saito, H. Cluster microRNAs miR-194 and miR-215 suppress the tumorigenicity of intestinal tumor organoids. Cancer Sci., 2017, 108(4), 678-684.
[88]
Jones, M.F.; Hara, T.; Francis, P.; Li, X.L.; Bilke, S.; Zhu, Y.; Pineda, M.; Subramanian, M.; Bodmer, W.F.; Lal, A. The CDX1-microRNA-215 axis regulates colorectal cancer stem cell differentiation. Proc. Natl. Acad. Sci. USA, 2015, 112(13), E1550-E1558.
[89]
Jiang, L.; Hermeking, H. miR-34a and miR-34b/c suppress intestinal tumorigenesis. Cancer Res., 2017, 77(10), 2746-2758.
[90]
Fantini, S.; Salsi, V.; Reggiani, L.; Maiorana, A.; Zappavigna, V. The miR-196b miRNA inhibits the GATA6 intestinal transcription factor and is upregulated in colon cancer patients. Oncotarget, 2017, 8(3), 4747-4759.
[91]
Zou, F.; Mao, R.; Yang, L.; Lin, S.; Lei, K.; Zheng, Y.; Ding, Y.; Zhang, P.; Cai, G.; Liang, X.; Liu, J. Targeted deletion of miR-139-5p activates MAPK, NF-kappaB and STAT3 signaling and promotes intestinal inflammation and colorectal cancer. FEBS J., 2016, 283(8), 1438-1452.
[92]
Yang, Y.; Weng, W.; Peng, J.; Hong, L.; Yang, L.; Toiyama, Y.; Gao, R.; Liu, M.; Yin, M.; Pan, C. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating toll-like receptor 4 signaling to nuclear factor−κB, and up-regulating expression of microRNA-21. Gastroenterology, 2017, 152(4), 851-866. e24.
[93]
Carvalho, J.; van Grieken, N.C.; Pereira, P.M.; Sousa, S.; Tijssen, M.; Buffart, T.E.; Diosdado, B.; Grabsch, H.; Santos, M.A.; Meijer, G.; Seruca, R.; Carvalho, B.; Oliveira, C. Lack of microRNA-101 causes E-cadherin functional deregulation through EZH2 up-regulation in intestinal gastric cancer. J. Pathol., 2012, 228(1), 31-44.
[94]
Sun, X.; Zhai, H.; Chen, X.; Kong, R.; Zhang, X. MicroRNA-1271 suppresses the proliferation and invasion of colorectal cancer cells by regulating metadherin/Wnt signaling. J. Biochem. Mol. Toxicol., 2018, 32(2)e22028
[95]
Tian, Y.; Pan, Q.; Shang, Y.; Zhu, R.; Ye, J.; Liu, Y.; Zhong, X.; Li, S.; He, Y.; Chen, L.; Zhao, J.; Chen, W.; Peng, Z.; Wang, R. MicroRNA-200 (miR-200) cluster regulation by achaete scute-like 2 (Ascl2): impact on the epithelial-mesenchymal transition in colon cancer cells. J. Biol. Chem., 2014, 289(52), 36101-36115.
[96]
Xu, L.; Li, M.; Wang, M.; Yan, D.; Feng, G.; An, G. The expression of microRNA-375 in plasma and tissue is matched in human colorectal cancer. BMC Cancer, 2014, 14, 714.
[97]
Liu, H.; Chen, Y.; Ming, D.; Wang, J.; Li, Z.; Ma, X.; Wang, J.; van Milgen, J.; Wang, F. Integrative analysis of indirect calorimetry and metabolomics profiling reveals alterations in energy metabolism between fed and fasted pigs. J. Anim. Sci. Biotechnol., 2018, 9, 41.


Rights & PermissionsPrintExport Cite as


Article Details

VOLUME: 20
ISSUE: 7
Year: 2019
Page: [666 - 673]
Pages: 8
DOI: 10.2174/1389203720666190125110626
Price: $58

Article Metrics

PDF: 13
HTML: 2
EPUB: 1
PRC: 1