90
Views
13
CrossRef citations to date
0
Altmetric
Review

MicroRNAs: Multifaceted Regulators of Colorectal Cancer Metastasis and Clinical Applications

ORCID Icon, ORCID Icon, , , , & ORCID Icon show all
Pages 10851-10866 | Published online: 27 Oct 2020

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69(1):7–34. doi:10.3322/caac.2155130620402
  • Miller KD, Nogueira L, Mariotto AB, et al. Cancer treatment and survivorship statistics, 2019. CA Cancer J Clin. 2019;69(5):363–385. doi:10.3322/caac.2156531184787
  • Smith RA, Andrews KS, Brooks D, et al. Cancer screening in the United States, 2019: a review of current American Cancer Society guidelines and current issues in cancer screening. CA Cancer J Clin. 2019;69(3):184–210. doi:10.3322/caac.2155730875085
  • Pretzsch E, Bosch F, Neumann J, et al. Mechanisms of metastasis in colorectal cancer and metastatic organotropism: hematogenous versus peritoneal spread. J Oncol. 2019;2019:7407190. doi:10.1155/2019/740719031641356
  • Pastushenko I, Blanpain C. EMT transition states during tumor progression and metastasis. Trends Cell Biol. 2019;29(3):212–226. doi:10.1016/j.tcb.2018.12.00130594349
  • Yuzhalin AE, Lim SY, Kutikhin AG, Gordon-Weeks AN. Dynamic matrisome: ECM remodeling factors licensing cancer progression and metastasis. Biochim Biophys Acta Rev Cancer. 2018;1870(2):207–228. doi:10.1016/j.bbcan.2018.09.00230316942
  • Soheilifar MH, Grusch M, Neghab HK, et al. Angioregulatory microRNAs in colorectal cancer. Cancers (Basel). 2019;12:1. doi:10.3390/cancers12010071
  • Zeng Z, Li Y, Pan Y, et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun. 2018;9(1):5395. doi:10.1038/s41467-018-07810-w30568162
  • Stacker SA, Achen MG, Jussila L, Baldwin ME, Alitalo K. Lymphangiogenesis and cancer metastasis. Nat Rev Cancer. 2002;2(8):573–583. doi:10.1038/nrc86312154350
  • Lambert AW, Pattabiraman DR, Weinberg RA. Emerging biological principles of metastasis. CELL. 2017;168(4):670–691. doi:10.1016/j.cell.2016.11.03728187288
  • Fares J, Fares MY, Khachfe HH, Salhab HA, Fares Y. Molecular principles of metastasis: a hallmark of cancer revisited. Signal Transduct Target Ther. 2020;5:28.32296047
  • Quintero-Fabian S, Arreola R, Becerril-Villanueva E, et al. Role of matrix metalloproteinases in angiogenesis and cancer. Front Oncol. 2019;9:1370. doi:10.3389/fonc.2019.0137031921634
  • Nandy SB, Lakshmanaswamy R. Cancer stem cells and metastasis. Prog Mol Biol Transl Sci. 2017;151:137–176.29096892
  • Raza U, Zhang JD, Sahin O. MicroRNAs: master regulators of drug resistance, stemness, and metastasis. J Mol Med (Berl). 2014;92(4):321–336. doi:10.1007/s00109-014-1129-224509937
  • Lu TX, Rothenberg ME. MicroRNA. J Allergy Clin Immunol. 2018;141(4):1202–1207. doi:10.1016/j.jaci.2017.08.03429074454
  • Baek D, Villen J, Shin C, et al. The impact of microRNAs on protein output. NATURE. 2008;455(7209):64–71. doi:10.1038/nature0724218668037
  • Garofalo M, Croce CM. microRNAs: master regulators as potential therapeutics in cancer. Annu Rev Pharmacol Toxicol. 2011;51:25–43. doi:10.1146/annurev-pharmtox-010510-10051720809797
  • Trepat X, Chen Z, Jacobson K. Cell migration. Compr Physiol. 2012;2(4):2369–2392.23720251
  • Fife CM, McCarroll JA, Kavallaris M. Movers and shakers: cell cytoskeleton in cancer metastasis. Br J Pharmacol. 2014;171(24):5507–5523. doi:10.1111/bph.1270424665826
  • Wu JI, Wang LH. Emerging roles of gap junction proteins connexins in cancer metastasis, chemoresistance and clinical application. J Biomed Sci. 2019;26(1):8.30642339
  • Wilson K, Lewalle A, Fritzsche M, Thorogate R, Duke T, Charras G. Mechanisms of leading edge protrusion in interstitial migration. NAT COMMUN. 2013;4:2896. doi:10.1038/ncomms389624305616
  • Kim CW, Oh ET, Kim JM, et al. Corrigendum to “Hypoxia-induced microRNA-590-5p promotes colorectal cancer progression by modulating matrix metalloproteinase activity” [Cancer Lett. 416 (2018) 31-41]. Cancer Lett. 2019;455::73. doi:10.1016/j.canlet.2019.04.02431060874
  • Julian L, Olson MF. Rho-associated coiled-coil containing kinases (ROCK): structure, regulation, and functions. Small GTPases. 2014;5:e29846. doi:10.4161/sgtp.2984625010901
  • Yu X, Wang D, Wang X, et al. CXCL12/CXCR4 promotes inflammation-driven colorectal cancer progression through activation of RhoA signaling by sponging miR-133a-3p. J Exp Clin Cancer Res. 2019;38(1):32. doi:10.1186/s13046-018-1014-x30678736
  • Zhuang M, Zhao S, Jiang Z, et al. MALAT1 sponges miR-106b-5p to promote the invasion and metastasis of colorectal cancer via SLAIN2 enhanced microtubules mobility. EBIOMEDICINE. 2019;41:286–298. doi:10.1016/j.ebiom.2018.12.04930797712
  • Liu H, Liu Y, Sun P, et al. Bai J and Cui B. Colorectal cancer-derived exosomal miR-106b-3p promotes metastasis by down-regulating DLC-1 expression. Clin Sci (Lond). 2020;134(4):419–434. doi:10.1042/CS2019108732065214
  • Sheng N, Tan G, You W, et al. MiR-145 inhibits human colorectal cancer cell migration and invasion via PAK4-dependent pathway. Cancer Med. 2017;6(6):1331–1340. doi:10.1002/cam4.102928440035
  • Wei AW, Li LF. Long non-coding RNA SOX21-AS1 sponges miR-145 to promote the tumorigenesis of colorectal cancer by targeting MYO6. Biomed Pharmacother. 2017;96:953–959. doi:10.1016/j.biopha.2017.11.14529217166
  • Anderson LR, Owens TW, Naylor MJ. Integrins in development and cancer. Biophys Rev. 2014;6(2):191–202.28510181
  • Barkan D, Chambers AF. beta1-integrin: a potential therapeutic target in the battle against cancer recurrence. Clin Cancer Res. 2011;17(23):7219–7223. doi:10.1158/1078-0432.CCR-11-064221900388
  • Yang X, Chen J, Liao Y, et al. MiR-27b-3p promotes migration and invasion in colorectal cancer cells by targeting HOXA10. Biosci Rep. 2019;39(12).
  • Zhao Y, Miao G, Li Y, et al. MicroRNA- 130b suppresses migration and invasion of colorectal cancer cells through downregulation of integrin beta1 [corrected]. PLoS One. 2014;9(2):e87938.24498407
  • Laudato S, Patil N, Abba ML, et al. 53-induced miR-30e-5p inhibits colorectal cancer invasion and metastasis by targeting ITGA6 and ITGB1. Int J Cancer. 2017;141(9):1879–1890. doi:10.1002/ijc.3085428656629
  • Huang L, Cai JL, Huang PZ, et al. miR19b-3p promotes the growth and metastasis of colorectal cancer via directly targeting ITGB8. Am J Cancer Res. 2017;7(10):1996–2008.29119049
  • Yoo HI, Kim BK, Yoon SK. MicroRNA-330-5p negatively regulates ITGA5 expression in human colorectal cancer. Oncol Rep. 2016;36(5):3023–3029. doi:10.3892/or.2016.509227633518
  • Liberti MV, Locasale JW. Correction to: ‘The Warburg Effect: how does it benefit cancer cells?’: [Trends in Biochemical Sciences, 41 (2016) 211]. Trends Biochem Sci. 2016;41(3):287. doi:10.1016/j.tibs.2016.01.00429482833
  • Barisciano G, Colangelo T, Rosato V, et al. Correction: miR-27a is a master regulator of metabolic reprogramming and chemoresistance in colorectal cancer. Br J Cancer. 2020.
  • Deng F, Zhou R, Lin C, et al. Tumor-secreted dickkopf2 accelerates aerobic glycolysis and promotes angiogenesis in colorectal cancer. Theranostics. 2019;9(4):1001–1014. doi:10.7150/thno.3005630867812
  • Wang X, Zhang H, Yang H, et al. Exosome-delivered circRNA promotes glycolysis to induce chemoresistance through the miR-122-PKM2 axis in colorectal cancer. Mol Oncol. 2020;14(3):539–555. doi:10.1002/1878-0261.1262931901148
  • Dongre A, Weinberg RA. New insights into the mechanisms of epithelial-mesenchymal transition and implications for cancer. Nat Rev Mol Cell Biol. 2019;20(2):69–84. doi:10.1038/s41580-018-0080-430459476
  • Vu T, Datta PK. Regulation of EMT in colorectal cancer: a culprit in metastasis. Cancers (Basel). 2017;9:12. doi:10.3390/cancers9120171
  • Li H, Rokavec M, Jiang L, Horst D, Hermeking H. Antagonistic Effects of p53 and HIF1A on microRNA-34a regulation of PPP1R11 and STAT3 and hypoxia-induced epithelial to mesenchymal transition in colorectal cancer cells. Gastroenterology. 2017;153(2):505–520. doi:10.1053/j.gastro.2017.04.01728435028
  • Liu Y, Gu Y, Cao X. The exosomes in tumor immunity. Oncoimmunology. 2015;4(9):e1027472.26405598
  • Ruiz-Lopez L, Blancas I, Garrido JM, et al. The role of exosomes on colorectal cancer: a review. J Gastroenterol Hepatol. 2018;33(4):792–799. doi:10.1111/jgh.1404929156509
  • Sanchez-Martin D, Otsuka A, Kabashima K, et al. Effects of DLC1 deficiency on endothelial cell contact growth inhibition and angiosarcoma progression. J Natl Cancer Inst. 2018;110(4):390–399. doi:10.1093/jnci/djx21929202196
  • Sun Z, Ou C, Liu J, et al. YAP1-induced MALAT1 promotes epithelial-mesenchymal transition and angiogenesis by sponging miR-126-5p in colorectal cancer. Oncogene. 2019;38(14):2627–2644. doi:10.1038/s41388-018-0628-y30531836
  • Ren LL, Yan TT, Shen CQ, et al. The distinct role of strand-specific miR-514b-3p and miR-514b-5p in colorectal cancer metastasis. Cell Death Dis. 2018;9(6):687. doi:10.1038/s41419-018-0732-529880874
  • Xie Y, Zhao J, Liang Y, et al. MicroRNA-10b controls the metastasis and proliferation of colorectal cancer cells by regulating Kruppel-like factor 4. Artif Cells Nanomed Biotechnol. 2019;47(1):1722–1729. doi:10.1080/21691401.2019.160600631032663
  • Tang W, Zhu Y, Gao J, et al. MicroRNA-29a promotes colorectal cancer metastasis by regulating matrix metalloproteinase 2 and E-cadherin via KLF4. Br J Cancer. 2014;110(2):450–458. doi:10.1038/bjc.2013.72424281002
  • Ding D, Li C, Zhao T, Li D, Yang L, Zhang B. LncRNA H19/miR-29b-3p/PGRN axis promoted epithelial-mesenchymal transition of colorectal cancer cells by acting on wnt signaling. Mol Cells. 2018;41(5):423–435.29754471
  • Li T, Jian X, He H, et al. MiR-452 promotes an aggressive colorectal cancer phenotype by regulating a Wnt/beta-catenin positive feedback loop. J Exp Clin Cancer Res. 2018;37(1):238. doi:10.1186/s13046-018-0879-z30253791
  • Bu P, Wang L, Chen KY, et al. miR-1269 promotes metastasis and forms a positive feedback loop with TGF-beta. Nat Commun. 2015;6:6879. doi:10.1038/ncomms787925872451
  • Zhao S, Sun H, Jiang W, et al. miR-4775 promotes colorectal cancer invasion and metastasis via the Smad7/TGFbeta-mediated epithelial to mesenchymal transition. Mol Cancer. 2017;16(1):12. doi:10.1186/s12943-017-0585-z28095858
  • Cai HK, Chen X, Tang YH, Deng YC. MicroRNA-194 modulates epithelial-mesenchymal transition in human colorectal cancer metastasis. Onco Targets Ther. 2017;10:1269–1278. doi:10.2147/OTT.S12517228280361
  • Sun J, Hu J, Wang G, et al. LncRNA TUG1 promoted KIAA1199 expression via miR-600 to accelerate cell metastasis and epithelial-mesenchymal transition in colorectal cancer. J Exp Clin Cancer Res. 2018;37(1):106. doi:10.1186/s13046-018-0771-x29776371
  • Shen Z, Zhou R, Liu C, et al. MicroRNA-105 is involved in TNF-alpha-related tumor microenvironment enhanced colorectal cancer progression. Cell Death Dis. 2017;8(12):3213. doi:10.1038/s41419-017-0048-x29238068
  • Shen T, Cheng X, Liu X, et al. Circ_0026344 restrains metastasis of human colorectal cancer cells via miR-183. Artif Cells Nanomed Biotechnol. 2019;47(1):4038–4045. doi:10.1080/21691401.2019.166962031608699
  • Geng Y, Zheng X, Hu W, et al. Hsa_circ_0009361 acts as the sponge of miR-582 to suppress colorectal cancer progression by regulating APC2 expression. Clin Sci (Lond). 2019;133(10):1197–1213. doi:10.1042/CS2019028631109967
  • Wang H, Yan B, Zhang P, et al. MiR-496 promotes migration and epithelial-mesenchymal transition by targeting RASSF6 in colorectal cancer. J Cell Physiol. 2020;235(2):1469–1479. doi:10.1002/jcp.2906631273789
  • Tang W, Hong L, Dai W, et al. MicroRNA500a5p inhibits colorectal cancer cell invasion and epithelialmesenchymal transition. INT J ONCOL. 2020.
  • Li J, Peng W, Yang P, et al. MicroRNA-1224-5p inhibits metastasis and epithelial-mesenchymal transition in colorectal cancer by targeting SP1-Mediated NF-kappaB signaling pathways. FRONT ONCOL. 2020;10:294. doi:10.3389/fonc.2020.0029432231999
  • Karimi DF, Amini R, Saidijam M, Najafi R. miR-200c, a tumor suppressor that modulate the expression of cancer stem cells markers and epithelial-mesenchymal transition in colorectal cancer. J Cell Biochem. 2018;119(7):6288–6295. doi:10.1002/jcb.2688029663476
  • Chen H, Xiao Q, Hu Y, et al. ANGPTL1 attenuates colorectal cancer metastasis by up-regulating microRNA-138. J Exp Clin Cancer Res. 2017;36(1):78. doi:10.1186/s13046-017-0548-728606130
  • Shen X, Jiang H, Chen Z, et al. MicroRNA-145 inhibits cell migration and invasion in colorectal cancer by targeting TWIST. Onco Targets Ther. 2019;12:10799–10809. doi:10.2147/OTT.S21614731849487
  • Chen J, Zhang H, Chen Y, et al. miR-598 inhibits metastasis in colorectal cancer by suppressing JAG1/Notch2 pathway stimulating EMT. Exp Cell Res. 2017;352(1):104–112. doi:10.1016/j.yexcr.2017.01.02228161537
  • Wang YB, Shi Q, Li G, Zheng JH, Lin J, Qiu W. MicroRNA-488 inhibits progression of colorectal cancer via inhibition of the mitogen-activated protein kinase pathway by targeting claudin-2. Am J Physiol Cell Physiol. 2019;316(1):C33–C47. doi:10.1152/ajpcell.00047.201830207785
  • Chen YC, Ou MC, Fang CW, Lee TH, Tzeng SL. High glucose concentrations negatively regulate the IGF1R/Src/ERK Axis through the MicroRNA-9 in colorectal cancer. Cells-Basel. 2019;8:4.
  • Karimi L, Zeinali T, Hosseinahli N, et al. miRNA-143 replacement therapy harnesses the proliferation and migration of colorectal cancer cells in vitro. J Cell Physiol. 2019;234(11):21359–21368. doi:10.1002/jcp.2874531032951
  • Ma W, Liu B, Li J, et al. MicroRNA-302c represses epithelial-mesenchymal transition and metastasis by targeting transcription factor AP-4 in colorectal cancer. Biomed Pharmacother. 2018;105:670–676. doi:10.1016/j.biopha.2018.06.02529906744
  • Lun W, Wu X, Deng Q, Zhi F. MiR-218 regulates epithelial-mesenchymal transition and angiogenesis in colorectal cancer via targeting CTGF. Cancer Cell Int. 2018;18:83. doi:10.1186/s12935-018-0575-229977158
  • Park YR, Seo SY, Kim SL, et al. MiRNA-206 suppresses PGE2-induced colorectal cancer cell proliferation, migration, and invasion by targetting TM4SF1. Biosci Rep. 2018;38:5. doi:10.1042/BSR20180664
  • Chen X, Zeng K, Xu M, et al. 53-induced miR-1249 inhibits tumor growth, metastasis, and angiogenesis by targeting VEGFA and HMGA2. Cell Death Dis. 2019;10(2):131. doi:10.1038/s41419-018-1188-330755600
  • Li J, Zhao LM, Zhang C, et al. The lncRNA FEZF1-AS1 promotes the progression of colorectal cancer through regulating OTX1 and targeting miR-30a-5p. Oncol Res. 2020;28(1):51–63. doi:10.3727/096504019X1561978396470031270006
  • Park YR, Kim SL, Lee MR, et al. MicroRNA-30a-5p (miR-30a) regulates cell motility and EMT by directly targeting oncogenic TM4SF1 in colorectal cancer. J Cancer Res Clin Oncol. 2017;143(10):1915–1927. doi:10.1007/s00432-017-2440-428528497
  • Du F, Cao T, Xie H, et al. KRAS Mutation-Responsive miR-139-5p inhibits colorectal cancer progression and is repressed by Wnt signaling. Theranostics. 2020;10(16):7335–7350. doi:10.7150/thno.4597132641995
  • Lin X, Wang S, Sun M, et al. Correction to: miR-195-5p/NOTCH2-mediated EMT modulates IL-4 secretion in colorectal cancer to affect M2-like TAM polarization. J Hematol Oncol. 2019;12(1):122. doi:10.1186/s13045-019-0810-x31757211
  • Wei C, Yang C, Wang S, et al. Crosstalk between cancer cells and tumor associated macrophages is required for mesenchymal circulating tumor cell-mediated colorectal cancer metastasis. Mol Cancer. 2019;18(1):64. doi:10.1186/s12943-019-0976-430927925
  • Fan L, Wu Y, Wang J. Sevoflurane inhibits the migration and invasion of colorectal cancer cells through regulating ERK/MMP-9 pathway by up-regulating miR-203. Eur J Pharmacol. 2019;850:43–52. doi:10.1016/j.ejphar.2019.01.02530685432
  • Zhang L, Dong Y, Zhu N, et al. microRNA-139-5p exerts tumor suppressor function by targeting NOTCH1 in colorectal cancer. MOL CANCER. 2014;13:124.24885920
  • Yu L, Lu Y, Han X, et al. microRNA −140-5p inhibits colorectal cancer invasion and metastasis by targeting ADAMTS5 and IGFBP5. Stem Cell Res Ther. 2016;7(1):180. doi:10.1186/s13287-016-0438-527906093
  • Hu JL, Wang W, Lan XL, et al. CAFs secreted exosomes promote metastasis and chemotherapy resistance by enhancing cell stemness and epithelial-mesenchymal transition in colorectal cancer. Mol Cancer. 2019;18(1):91. doi:10.1186/s12943-019-1019-x31064356
  • Ren J, Ding L, Zhang D, et al. Carcinoma-associated fibroblasts promote the stemness and chemoresistance of colorectal cancer by transferring exosomal lncRNA H19. THERANOSTICS. 2018;8(14):3932–3948. doi:10.7150/thno.2554130083271
  • Viallard C, Larrivee B. Tumor angiogenesis and vascular normalization: alternative therapeutic targets. ANGIOGENESIS. 2017;20(4):409–426. doi:10.1007/s10456-017-9562-928660302
  • Xu Z, Zhu C, Chen C, et al. CCL19 suppresses angiogenesis through promoting miR-206 and inhibiting Met/ERK/Elk-1/HIF-1alpha/VEGF-A pathway in colorectal cancer. Cell Death Dis. 2018;9(10):974.30250188
  • Yamakuchi M, Lotterman CD, Bao C, et al. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci U S A. 2010;107(14):6334–6339. doi:10.1073/pnas.091108210720308559
  • Melincovici CS, Bosca AB, Susman S, et al. Vascular endothelial growth factor (VEGF) - key factor in normal and pathological angiogenesis. Rom J Morphol Embryol. 2018;59(2):455–467.30173249
  • Hu HY, Yu CH, Zhang HH, et al. Exosomal miR-1229 derived from colorectal cancer cells promotes angiogenesis by targeting HIPK2. Int J Biol Macromol. 2019;132:470–477.30936013
  • Guan H, Xie L, Leithauser F, et al. KLF4 is a tumor suppressor in B-cell non-Hodgkin lymphoma and in classic Hodgkin lymphoma. Blood. 2010;116(9):1469–1478. doi:10.1182/blood-2009-12-25644620519630
  • Yamada NO, Heishima K, Akao Y, Senda T. Extracellular vesicles containing MicroRNA-92a-3p facilitate partial endothelial-mesenchymal transition and angiogenesis in endothelial cells. Int J Mol Sci. 2019;20:18. doi:10.3390/ijms20184406
  • Xu Q, Tong JL, Zhang CP, Xiao Q, Lin XL, Xiao XY. miR-27a induced by colon cancer cells in HLECs promotes lymphangiogenesis by targeting SMAD4. PLoS One. 2017;12(10):e186718.
  • Fabisiewicz A, Grzybowska E. CTC clusters in cancer progression and metastasis. Med Oncol. 2017;34(1):12. doi:10.1007/s12032-016-0875-028012133
  • Simpson CD, Anyiwe K, Schimmer AD. Anoikis resistance and tumor metastasis. Cancer Lett. 2008;272(2):177–185. doi:10.1016/j.canlet.2008.05.02918579285
  • Sa KD, Zhang X, Li XF, et al. A miR-124/ITGA3 axis contributes to colorectal cancer metastasis by regulating anoikis susceptibility. Biochem Biophys Res Commun. 2018;501(3):758–764. doi:10.1016/j.bbrc.2018.05.06229758195
  • Liu Y, Zhang Y, Wu H, et al. Mir-10a suppresses colorectal cancer metastasis by modulating the epithelial-to-mesenchymal transition and anoikis. Cell Death Dis. 2017;8(4):e2739. doi:10.1038/cddis.2017.6128383561
  • Carter L, Fouser LA, Jussif J, et al. PD-1:PD-Linhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur J Immunol. 2002;32(3):634–643. doi:10.1002/1521-4141(200203)32:3<634::AID-IMMU634>3.0.CO;2-911857337
  • Chen YL, Wang GX, Lin BA, Huang JS. MicroRNA-93-5p expression in tumor tissue and its tumor suppressor function via targeting programmed death ligand-1 in colorectal cancer. Cell Biol Int. 2020;44(5):1224–1236. doi:10.1002/cbin.1132332068322
  • Peinado H, Zhang H, Matei IR, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer. 2017;17(5):302–317.28303905
  • Paget S. The distribution of secondary growths in cancer of the breast. 1889 Cancer Metastasis Rev. 1989;8(2):98–101.2673568
  • Shao Y, Chen T, Zheng X, et al. Colorectal cancer-derived small extracellular vesicles establish an inflammatory premetastatic niche in liver metastasis. Carcinogenesis. 2018;39(11):1368–1379. doi:10.1093/carcin/bgy11530184100
  • Wang D, Wang X, Si M, et al. Exosome-encapsulated miRNAs contribute to CXCL12/CXCR4-induced liver metastasis of colorectal cancer by enhancing M2 polarization of macrophages. Cancer Lett. 2020;474:36–52. doi:10.1016/j.canlet.2020.01.00531931030
  • Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9(4):265–273. doi:10.1038/nrc262019262571
  • Hur K, Toiyama Y, Takahashi M, et al. MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis. Gut. 2013;62(9):1315–1326. doi:10.1136/gutjnl-2011-30184622735571
  • Adorno-Cruz V, Kibria G, Liu X, et al. Cancer stem cells: targeting the roots of cancer, seeds of metastasis, and sources of therapy resistance. Cancer Res. 2015;75(6):924–929. doi:10.1158/0008-5472.CAN-14-322525604264
  • Jiao X, Qian X, Wu L, et al. microRNA: the impact on cancer stemness and therapeutic resistance. Cells-Basel. 2019;9:1.
  • Wang L, Bu P, Ai Y, et al. A long non-coding RNA targets microRNA miR-34a to regulate colon cancer stem cell asymmetric division. Elife. 2016;5.
  • Cheng WC, Liao TT, Lin CC, et al. RAB27B-activated secretion of stem-like tumor exosomes delivers the biomarker microRNA-146a-5p, which promotes tumorigenesis and associates with an immunosuppressive tumor microenvironment in colorectal cancer. Int J Cancer. 2019;145(8):2209–2224. doi:10.1002/ijc.3233830980673
  • Sun L, Fang Y, Wang X, et al. miR-302a inhibits metastasis and cetuximab resistance in colorectal cancer by targeting NFIB and CD44. Theranostics. 2019;9(26):8409–8425. doi:10.7150/thno.3660531754405
  • Fan D, Lin X, Zhang F, et al. MicroRNA 26b promotes colorectal cancer metastasis by downregulating phosphatase and tensin homolog and wingless-type MMTV integration site family member 5A. Cancer Sci. 2018;109(2):354–362. doi:10.1111/cas.1345129160937
  • Wang LQ, Yu P, Li B, et al. miR-372 and miR-373 enhance the stemness of colorectal cancer cells by repressing differentiation signaling pathways. Mol Oncol. 2018;12(11):1949–1964. doi:10.1002/1878-0261.1237630171794
  • Mukohyama J, Isobe T, Hu Q, et al. miR-221 targets QKI to enhance the tumorigenic capacity of human colorectal cancer stem cells. Cancer Res. 2019;79(20):5151–5158. doi:10.1158/0008-5472.CAN-18-354431416845
  • Yu Y, Kanwar SS, Patel BB, et al. MicroRNA-21 induces stemness by downregulating transforming growth factor beta receptor 2 (TGFbetaR2) in colon cancer cells. Carcinogenesis. 2012;33(1):68–76. doi:10.1093/carcin/bgr24622072622
  • Lai HT, Tseng WK, Huang SW, Chao TC, Su Y. MicroRNA-203 diminishes the stemness of human colon cancer cells by suppressing GATA6 expression. J Cell Physiol. 2020;235(3):2866–2880. doi:10.1002/jcp.2919231544978
  • Jiang S, Miao D, Wang M, Lv J, Wang Y, Tong J. MiR-30-5p suppresses cell chemoresistance and stemness in colorectal cancer through USP22/Wnt/beta-catenin signaling axis. J Cell Mol Med. 2019;23(1):630–640. doi:10.1111/jcmm.1396830338942
  • Ma X, Liu J, Li J, et al. miR-139-5p reverses stemness maintenance and metastasis of colon cancer stem-like cells by targeting E2-2. J Cell Physiol. 2019;234(12):22703–22718. doi:10.1002/jcp.2883631120140
  • Jin Y, Wang M, Hu H, Huang Q, Chen Y, Wang G. Overcoming stemness and chemoresistance in colorectal cancer through miR-195-5p-modulated inhibition of notch signaling. Int J Biol Macromol. 2018;117:445–453. doi:10.1016/j.ijbiomac.2018.05.15129852230
  • Yu Y, Nangia-Makker P, Farhana L, Majumdar A. A novel mechanism of lncRNA and miRNA interaction: CCAT2 regulates miR-145 expression by suppressing its maturation process in colon cancer cells. Mol Cancer. 2017;16(1):155. doi:10.1186/s12943-017-0725-528964256
  • Tang D, Yang Z, Long F, et al. Long noncoding RNA MALAT1 mediates stem cell-like properties in human colorectal cancer cells by regulating miR-20b-5p/Oct4 axis. J Cell Physiol. 2019;234(11):20816–20828. doi:10.1002/jcp.2868731012108
  • Chen DL, Lu YX, Zhang JX, et al. Long non-coding RNA UICLM promotes colorectal cancer liver metastasis by acting as a ceRNA for microRNA-215 to regulate ZEB2 expression. THERANOSTICS. 2017;7(19):4836–4849. doi:10.7150/thno.2094229187907
  • Khodadadi KA, Saidijam M, Amini R, Samadi P, Najafi R. Induction of let-7e gene expression attenuates oncogenic phenotype in HCT-116 colorectal cancer cells through targeting of DCLK1 regulation. Life Sci. 2019;228:221–227. doi:10.1016/j.lfs.2019.05.00531075231
  • Ji D, Zhan T, Li M, et al. Enhancement of sensitivity to chemo/radiation therapy by using miR-15b against DCLK1 in colorectal cancer. Stem Cell Rep. 2018;11(6):1506–1522. doi:10.1016/j.stemcr.2018.10.015
  • Hong YG, Xin C, Zheng H, et al. miR-365a-3p regulates ADAM10-JAK-STAT signaling to suppress the growth and metastasis of colorectal cancer cells. J Cancer. 2020;11(12):3634–3644. doi:10.7150/jca.4273132284760
  • Bukowski K, Kciuk M, Kontek R. Mechanisms of multidrug resistance in cancer chemotherapy. INT J MOL SCI. 2020;21:9. doi:10.3390/ijms21093233
  • Xu F, Ye ML, Zhang YP, et al. MicroRNA-375-3p enhances chemosensitivity to 5-fluorouracil by targeting thymidylate synthase in colorectal cancer. Cancer Sci. 2020;111(5):1528–1541. doi:10.1111/cas.1435632073706
  • Kannathasan T, Kuo WW, Chen MC, et al. Chemoresistance-associated silencing of miR-4454 promotes colorectal cancer aggression through the GNL3L and NF-kappaB pathway. Cancers (Basel). 2020;12:5. doi:10.3390/cancers12051231
  • Liu T, Zhang X, Du L, et al. Exosome-transmitted miR-128-3p increase chemosensitivity of oxaliplatin-resistant colorectal cancer. Mol Cancer. 2019;18(1):43. doi:10.1186/s12943-019-0981-730890168
  • Tang Y, Zhao Y, Song X, Song X, Niu L, Xie L. Tumor-derived exosomal miRNA-320d as a biomarker for metastatic colorectal cancer. J Clin Lab Anal. 2019;33(9):e23004. doi:10.1002/jcla.2300431420913
  • Sun Y, Yang B, Lin M, et al. Identification of serum miR-30a-5p as a diagnostic and prognostic biomarker in colorectal cancer. Cancer Biomark. 2019;24(3):299–305. doi:10.3233/CBM-18212930829615
  • Sabry D, El-Deek S, Maher M, et al. Role of miRNA-210, miRNA-21 and miRNA-126 as diagnostic biomarkers in colorectal carcinoma: impact of HIF-1alpha-VEGF signaling pathway. Mol Cell Biochem. 2019;454(1–2):177–189.30357530
  • Choi HH, Cho YS, Choi JH, Kim HK, Kim SS, Chae HS. Stool-Based miR-92a and miR-144* as noninvasive biomarkers for colorectal cancer screening. Oncology. 2019;97(3):173–179. doi:10.1159/00050063931216561
  • Ulivi P, Canale M, Passardi A, et al. Circulating plasma levels of miR-20b, miR-29b and miR-155 as predictors of bevacizumab efficacy in patients with metastatic colorectal cancer. Int J Mol Sci. 2018;19:1. doi:10.3390/ijms19010307
  • Zhang Y, Liu X, Zhang J, et al. Inhibition of miR-19a partially reversed the resistance of colorectal cancer to oxaliplatin via PTEN/PI3K/AKT pathway. Aging (Albany NY). 2020;12(7):5640–5650. doi:10.18632/aging.10292932209726
  • Liang H, Xu Y, Zhang Q, et al. MiR-483-3p regulates oxaliplatin resistance by targeting FAM171B in human colorectal cancer cells. Artif Cells Nanomed Biotechnol. 2019;47(1):725–736. doi:10.1080/21691401.2019.156953030861353
  • Liu N, Li J, Zhao Z, et al. MicroRNA-302a enhances 5-fluorouracil-induced cell death in human colon cancer cells. Oncol Rep. 2017;37(1):631–639. doi:10.3892/or.2016.523727840990
  • Meng X, Fu R. miR-206 regulates 5-FU resistance by targeting Bcl-2 in colon cancer cells. Onco Targets Ther. 2018;11:1757–1765. doi:10.2147/OTT.S15909329636622
  • Hsu HH, Kuo WW, Shih HN, et al. FOXC1 regulation of miR-31-5p confers oxaliplatin resistance by targeting LATS2 in colorectal cancer. Cancers (Basel). 2019;11:10. doi:10.3390/cancers11101576
  • Wang M, Han D, Yuan Z, et al. Long non-coding RNA H19 confers 5-Fu resistance in colorectal cancer by promoting SIRT1-mediated autophagy. Cell Death Dis. 2018;9(12):1149. doi:10.1038/s41419-018-1187-430451820
  • Yu X, Shi W, Zhang Y, et al. CXCL12/CXCR4 axis induced miR-125b promotes invasion and confers 5-fluorouracil resistance through enhancing autophagy in colorectal cancer. Sci Rep. 2017;7:42226. doi:10.1038/srep4222628176874
  • Brabletz T, Jung A, Reu S, et al. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci U S A. 2001;98(18):10356–10361. doi:10.1073/pnas.17161049811526241
  • Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100(7):3983–3988. doi:10.1073/pnas.053029110012629218
  • Fabregat I, Malfettone A, Soukupova J. New insights into the crossroads between EMT and stemness in the context of cancer. J Clin Med. 2016;5:3. doi:10.3390/jcm5030037
  • Lan L, Luo Y, Cui D, et al. Epithelial-mesenchymal transition triggers cancer stem cell generation in human thyroid cancer cells. Int J Oncol. 2013;43(1):113–120. doi:10.3892/ijo.2013.191323604232
  • Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834–838. doi:10.1038/nature0370215944708
  • Rosenfeld N, Aharonov R, Meiri E, et al. MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol. 2008;26(4):462–469. doi:10.1038/nbt139218362881
  • Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A. 2006;103(7):2257–2261. doi:10.1073/pnas.051056510316461460
  • Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014;15(8):509–524.25027649
  • Ou C, Sun Z, Li X, et al. MiR-590-5p, a density-sensitive microRNA, inhibits tumorigenesis by targeting YAP1 in colorectal cancer. Cancer Lett. 2017;399:53–63. doi:10.1016/j.canlet.2017.04.01128433598
  • Kogure A, Kosaka N, Ochiya T. Cross-talk between cancer cells and their neighbors via miRNA in extracellular vesicles: an emerging player in cancer metastasis. J Biomed Sci. 2019;26(1):7. doi:10.1186/s12929-019-0500-630634952
  • Yang F, Ning Z, Ma L, et al. Exosomal miRNAs and miRNA dysregulation in cancer-associated fibroblasts. Mol Cancer. 2017;16(1):148.28851377
  • Islam MS, Ciavattini A, Petraglia F, Castellucci M, Ciarmela P. Extracellular matrix in uterine leiomyoma pathogenesis: a potential target for future therapeutics. Hum Reprod Update. 2018;24(1):59–85.29186429
  • Wang J, Ni J, Beretov J, Thompson J, Graham P, Li Y. Exosomal microRNAs as liquid biopsy biomarkers in prostate cancer. Crit Rev Oncol Hematol. 2020;145:102860. doi:10.1016/j.critrevonc.2019.10286031874447
  • Joyce DP, Kerin MJ, Dwyer RM. Exosome-encapsulated microRNAs as circulating biomarkers for breast cancer. Int J Cancer. 2016;139(7):1443–1448. doi:10.1002/ijc.3017927170104
  • Liang G, Zhu Y, Ali DJ, et al. Engineered exosomes for targeted co-delivery of miR-21 inhibitor and chemotherapeutics to reverse drug resistance in colon cancer. J Nanobiotechnology. 2020;18(1):10.31918721