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Molecular Cancer
Published in: Molecular Cancer 1/2016

Open Access 01-12-2016 | Review

Wnt-signalling pathways and microRNAs network in carcinogenesis: experimental and bioinformatics approaches

Authors: Emenike K. Onyido, Eloise Sweeney, Abdolrahman Shams Nateri

Published in: Molecular Cancer | Issue 1/2016

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Abstract

Over the past few years, microRNAs (miRNAs) have not only emerged as integral regulators of gene expression at the post-transcriptional level but also respond to signalling molecules to affect cell function(s). miRNAs crosstalk with a variety of the key cellular signalling networks such as Wnt, transforming growth factor-β and Notch, control stem cell activity in maintaining tissue homeostasis, while if dysregulated contributes to the initiation and progression of cancer. Herein, we overview the molecular mechanism(s) underlying the crosstalk between Wnt-signalling components (canonical and non-canonical) and miRNAs, as well as changes in the miRNA/Wnt-signalling components observed in the different forms of cancer. Furthermore, the fundamental understanding of miRNA-mediated regulation of Wnt-signalling pathway and vice versa has been significantly improved by high-throughput genomics and bioinformatics technologies. Whilst, these approaches have identified a number of specific miRNA(s) that function as oncogenes or tumour suppressors, additional analyses will be necessary to fully unravel the links among conserved cellular signalling pathways and miRNAs and their potential associated components in cancer, thereby creating therapeutic avenues against tumours. Hence, we also discuss the current challenges associated with Wnt-signalling/miRNAs complex and the analysis using the biomedical experimental and bioinformatics approaches.
Literature
1.
2.
Novellasdemunt L, Antas P, Li VS. Targeting Wnt signaling in colorectal cancer. A Review in the Theme: Cell Signaling: Proteins, Pathways and Mechanisms. Am J Phys Cell Phys. 2015;309(8):C511–21.CrossRef
3.
4.
Sheikh A, et al. The role of Wnt signaling pathway in carcinogenesis and implications for anticancer. Hered Cancer Clin Pract. 2014;12(1):12–13.
5.
6.
Yang X, et al. Wnt signaling through Snail1 and Zeb1 regulates bone metastasis in lung cancer. Am J Cancer Res. 2015;5(2):748.PubMedPubMedCentral
7.
8.
9.
Miller JR, et al. Mechanism and function of signal transduction by the Wnt/beta-catenin and Wnt/Ca2+ pathways. Oncogene. 1999;18(55):7860–72.PubMedCrossRef
10.
11.
Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer. 2013;13(1):11–26.PubMedCrossRef
12.
Kim W, Kim M, Jho E-h. Wnt/β-catenin signalling: from plasma membrane to nucleus. Biochem J. 2013;450(1):9–21.PubMedCrossRef
13.
Rao TP, Kühl M. An Updated Overview on Wnt Signaling Pathways A Prelude for More. Circ Res. 2010;106(12):1798–806.PubMedCrossRef
14.
Aoki K, Taketo MM. Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J Cell Sci. 2007;120(19):3327–35.PubMedCrossRef
15.
16.
Wantae K, Minseong K, Eek-hoon J. Wnt/beta-catenin signalling: from plasma membrane to nucleus. Biochem J. 2013;450(1):9–21.CrossRef
17.
18.
Augsten M. Cancer-associated fibroblasts as another polarized cell type of the tumor microenvironment. Front Oncol. 2014;4(62):1–8.
19.
Sobel K, et al. Wnt‐3a‐activated human fibroblasts promote human keratinocyte proliferation and matrix destruction. Int J Cancer. 2015;136(12):2786–98.PubMedCrossRef
20.
Zeng X, et al. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development. 2008;135(2):367–75.PubMedCrossRef
21.
Bilić J, et al. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science. 2007;316(5831):1619–22.PubMedCrossRef
22.
23.
Angers S, Moon RT. Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol. 2009;10(7):468–77.PubMedCrossRef
24.
25.
Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004;20:781–810.PubMedCrossRef
26.
Pinto D, et al. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 2003;17(14):1709–13.
27.
Nateri AS, Spencer-Dene B, Behrens A. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature. 2005;437(7056):281–5.PubMedCrossRef
28.
Schwartz AL, et al. Phenylmethimazole decreases Toll-like receptor 3 and noncanonical Wnt5a expression in pancreatic cancer and melanoma together with tumor cell growth and migration. Clin Cancer Res. 2009;15(12):4114–22.PubMedPubMedCentralCrossRef
29.
Schlange T, et al. Autocrine WNT signaling contributes to breast cancer cell proliferation via the canonical WNT pathway and EGFR transactivation. Breast Cancer Res. 2007;9(5):1.CrossRef
30.
31.
Schlessinger K, McManus EJ, Hall A. Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J Cell Biol. 2007;178(3):355–61.PubMedPubMedCentralCrossRef
32.
Kikuchi A, et al. New insights into the mechanism of Wnt signaling pathway activation. Int Rev Cell Mol Biol. 2011;291(21):e71.
33.
Sugimura R, Li L. Noncanonical Wnt signaling in vertebrate development, stem cells, and diseases. Birth Defects Research Part C: Embryo Today: Reviews. 2010;90(4):243–56.CrossRef
34.
Sato A, et al. Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J. 2010;29(1):41–54.PubMedCrossRef
35.
Saadeddin A, et al. The links between transcription, beta-catenin/JNK signaling, and carcinogenesis. Mol Cancer Res. 2009;7(8):1189–96.PubMedCrossRef
36.
Ishitani T, et al. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca2+ pathway to antagonize Wnt/β-catenin signaling. Mol Cell Biol. 2003;23(1):131–9.PubMedPubMedCentralCrossRef
37.
Saneyoshi T, et al. The Wnt/calcium pathway activates NF-AT and promotes ventral cell fate in Xenopus embryos. Nature. 2002;417(6886):295–9.PubMedCrossRef
38.
Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer. 2008;8(5):387–98.PubMedCrossRef
39.
Sherwood V. WNT signaling: an emerging mediator of cancer cell metabolism? Mol Cell Biol. 2015;35(1):2–10.PubMedCrossRef
40.
Holland JD, et al. Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol. 2013;25(2):254–64.PubMedCrossRef
41.
Lee S-Y, et al. Mutation spectrum in the Wnt/β-catenin signaling pathway in gastric fundic gland-associated neoplasms/polyps. Virchows Arch. 2015;467(1):27–38.PubMedCrossRef
42.
Abdelmaksoud-Damak R, et al. Expression and Mutation Pattern of β-Catenin and Adenomatous Polyposis Coli in Colorectal Cancer Patients. Arch Med Res. 2015;46(1):54–62.PubMedCrossRef
43.
Satoh S, et al. AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat Genet. 2000;24(3):245–50.PubMedCrossRef
44.
45.
Samowitz WS, et al. APC mutations and other genetic and epigenetic changes in colon cancer. Mol Cancer Res. 2007;5(2):165–70.PubMedCrossRef
46.
Lüchtenborg M, et al. Mutations in APC, CTNNB1 and K-ras genes and expression of hMLH1 in sporadic colorectal carcinomas from the Netherlands Cohort Study. BMC Cancer. 2005;5(1):1.CrossRef
47.
Morikawa T, et al. Association of CTNNB1 (β-catenin) alterations, body mass index, and physical activity with survival in patients with colorectal cancer. JAMA. 2011;305(16):1685–94.PubMedPubMedCentralCrossRef
48.
You XJ, et al. Expression of Wnt pathway components frizzled and disheveled in colon cancer arising in patients with inflammatory bowel disease. Oncol Rep. 2007;18(3):691–4.PubMed
49.
50.
Cai X, Hagedorn CH, Cullen BR. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA. 2004;10(12):1957–66.PubMedPubMedCentralCrossRef
51.
Förstemann K, et al. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 2005;3(7):e236.PubMedPubMedCentralCrossRef
52.
53.
54.
Meister G, Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature. 2004;431(7006):343–9.PubMedCrossRef
55.
Meister G. Argonaute proteins: functional insights and emerging roles. Nat Rev Genet. 2013;14(7):447–59.
56.
57.
58.
59.
60.
61.
Vimalraj S, Selvamurugan N. MicroRNAs: synthesis, gene regulation and osteoblast differentiation. Curr Issues Mol Biol. 2012;15(1):7–18.PubMed
62.
63.
64.
65.
Medici D, Hay ED, Olsen BR. Snail and Slug promote epithelial-mesenchymal transition through betacatenin-T-cell factor-4-dependent expression of transforming growth factor-beta3. Mol Biol Cell. 2008;19(11):4875–4887.
66.
YIN JJ, POLLOCK CB, KELLY K. Mechanisms of cancer metastasis to the bone. Cell Res. 2005;15(1):57–62.PubMedCrossRef
67.
Müller A, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature. 2001;410(6824):50–6.PubMedCrossRef
68.
Kang Y, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 2003;3(6):537–49.PubMedCrossRef
69.
Zhang X, et al. MicroRNA-410 acts as oncogene in NSCLC through downregulating SLC34A2 via activating Wnt/β-catenin pathway. Oncotarget. 2016;7(12):14569–85.PubMedPubMedCentral
70.
Saydam O, et al. Downregulated microRNA-200a in meningiomas promotes tumor growth by reducing E-cadherin and activating the Wnt/β-catenin signaling pathway. Mol Cell Biol. 2009;29(21):5923–40.PubMedPubMedCentralCrossRef
71.
Kim NH, et al. p53 regulates nuclear GSK-3 levels through miR-34-mediated Axin2 suppression in colorectal cancer cells. Cell Cycle. 2013;12(10):1578–87.PubMedPubMedCentralCrossRef
72.
73.
Wang X, et al. MiR-214 inhibits cell growth in hepatocellular carcinoma through suppression of β-catenin. Biochem Biophys Res Commun. 2012;428(4):525–31.PubMedCrossRef
74.
Williams Z, et al. Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Proc Natl Acad Sci. 2013;110(11):4255–60.PubMedPubMedCentralCrossRef
75.
Du WW, et al. MicroRNA miR-24 enhances tumor invasion and metastasis by targeting PTPN9 and PTPRF to promote EGF signaling. J Cell Sci. 2013;126(6):1440–53.PubMedCrossRef
76.
77.
Su W-L, Kleinhanz RR, Schadt EE. Characterizing the role of miRNAs within gene regulatory networks using integrative genomics techniques. Mol Syst Biol. 2011;7(490):1–12.
78.
Chen TH, et al. The prognostic significance of APC gene mutation and miR‐21 expression in advanced‐stage colorectal cancer. Color Dis. 2013;15(11):1367–74.CrossRef
79.
Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 1992;52(6):1399–405.PubMed
80.
81.
Liu Y, et al. MicroRNAs modulate the Wnt signaling pathway through targeting its inhibitors. Biochem Biophys Res Commun. 2011;408(2):259–64.PubMedCrossRef
82.
83.
Sun X, et al. MiR-208a stimulates the cocktail of SOX2 and β-catenin to inhibit the let-7 induction of self-renewal repression of breast cancer stem cells and formed miR208a/let-7 feedback loop via LIN28 and DICER1. Oncotarget. 2015;6(32):32944–54.
84.
Wang D, et al. Human microRNA oncogenes and tumor suppressors show significantly different biological patterns: from functions to targets. PLoS One. 2010;5(9):e13067.PubMedPubMedCentralCrossRef
85.
86.
Nguyen LV, et al. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12(2):133–43.PubMed
87.
Ibrahim EE, et al. Embryonic NANOG activity defines colorectal cancer stem cells and modulates through AP1- and TCF-dependent mechanisms. Stem Cells. 2012;30(10):2076–87.PubMedCrossRef
88.
Yang K, et al. The evolving roles of canonical WNT signaling in stem cells and tumorigenesis: implications in targeted cancer therapies. Lab Invest. 2015;96(2):116–36.
89.
Sato N, et al. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med. 2004;10(1):55–63.PubMedCrossRef
90.
91.
Day TF, et al. Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell. 2005;8(5):739–50.PubMedCrossRef
92.
Gregorieff A, et al. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology. 2005;129(2):626–38.PubMedCrossRef
93.
Deng H, et al. miR-193a-3p regulates the multi-drug resistance of bladder cancer by targeting the LOXL4 gene and the Oxidative Stress pathway. Mol Cancer. 2014;13(1):234.PubMedPubMedCentralCrossRef
94.
Bitarte N, et al. MicroRNA‐451 Is Involved in the Self‐renewal, Tumorigenicity, and Chemoresistance of Colorectal Cancer Stem Cells. Stem Cells. 2011;29(11):1661–71.PubMedCrossRef
95.
de Sousa EMF, et al. Targeting Wnt signaling in colon cancer stem cells. Clin Cancer Res. 2011;17(4):647–53.PubMedCrossRef
96.
97.
98.
Takahashi R-U, Miyazaki H, Ochiya T. The role of microRNAs in the regulation of cancer stem cells. Front Genet. 2014;4(295):1–11.
99.
100.
101.
Ghahhari NM, Babashah S. Interplay between microRNAs and WNT/β-catenin signalling pathway regulates epithelial–mesenchymal transition in cancer. Eur J Cancer. 2015;51(12):1638–49.PubMedCrossRef
102.
Tam S, et al. Robust global microRNA expression profiling using next-generation sequencing technologies. Lab Investig. 2014;94(3):350–8.PubMedCrossRef
103.
Harris SR, et al. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis. 2013;13(2):130–6.PubMedPubMedCentralCrossRef
104.
Mortazavi A, et al. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5(7):621–8.PubMedCrossRef
105.
Pan Q, et al. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet. 2008;40(12):1413–5.PubMedCrossRef
106.
Johnson DS, et al. Genome-wide mapping of in vivo protein-DNA interactions. Science. 2007;316(5830):1497–502.PubMedCrossRef
107.
108.
Brunner AL, et al. Distinct DNA methylation patterns characterize differentiated human embryonic stem cells and developing human fetal liver. Genome Res. 2009;19(6):1044–56.PubMedPubMedCentralCrossRef
109.
110.
Kang H, Hata A. The role of microRNAs in cell fate determination of mesenchymal stem cells: balancing adipogenesis and osteogenesis. BMB Rep. 2015;48(6):319.PubMedPubMedCentralCrossRef
111.
Hassan MQ, et al. miR-218 directs a Wnt signaling circuit to promote differentiation of osteoblasts and osteomimicry of metastatic cancer cells. J Biol Chem. 2012;287(50):42084–92.PubMedPubMedCentralCrossRef
112.
113.
Yang J-H, et al. ChIPBase: a database for decoding the transcriptional regulation of long non-coding RNA and microRNA genes from ChIP-Seq data. Nucleic Acids Res. 2013;41(D1):D177–87.PubMedCrossRef
114.
Hoffmeyer K, et al. Wnt/β-catenin signaling regulates telomerase in stem cells and cancer cells. Science. 2012;336(6088):1549–54.PubMedCrossRef
115.
Blahnik KR, et al. Sole-Search: an integrated analysis program for peak detection and functional annotation using ChIP-seq data. Nucleic Acids Res. 2010;38(3):e13.PubMedCrossRef
116.
Zhang B, et al. Analysis of differentially expressed genes in ductal carcinoma with DNA microarray. Eur Rev Med Pharmacol Sci. 2013;17(6):758–66.PubMed
117.
118.
119.
120.
Bräutigam C, Raggioli A, Winter J. The Wnt/β-catenin pathway regulates the expression of the miR-302 cluster in mouse ESCs and P19 cells. PLoS One. 2013;8(9):e75315.PubMedPubMedCentralCrossRef
121.
Solberg N, et al. Mouse Tcf3 represses canonical Wnt signaling by either competing for β-catenin binding or through occupation of DNA-binding sites. Mol Cell Biochem. 2012;365(1–2):53–63.PubMedCrossRef
122.
Schepeler T, et al. Attenuation of the beta-catenin/TCF4 complex in colorectal cancer cells induces several growth-suppressive microRNAs that target cancer promoting genes. Oncogene. 2012;31(22):2750–60.PubMedCrossRef
123.
Tzeng S-L, et al. Physiological and functional interactions between Tcf4 and Daxx in colon cancer cells. J Biol Chem. 2006;281(22):15405–11.PubMedCrossRef
124.
125.
Pellegrini M, Ferrari R. Epigenetic analysis: ChIP-chip and ChIP-seq. Methods Mol Biol. 2012;802:377–387.
126.
127.
128.
Eminaga S, et al. Quantification of microRNA Expression with Next‐Generation Sequencing. Curr Protoc Mol Biol. 2013;Chapter 4:Unit 4.17.
129.
Liu J, et al. Next generation sequencing for profiling expression of miRNAs: technical progress and applications in drug development. J Biomed Sci Eng. 2011;4(10):666.PubMedPubMedCentralCrossRef
130.
Müller S, et al. Next-generation sequencing reveals novel differentially regulated mRNAs, lncRNAs, miRNAs, sdRNAs and a piRNA in pancreatic cancer. Mol Cancer. 2015;14(1):1.CrossRef
131.
Müller S, et al. omiRas: a Web server for differential expression analysis of miRNAs derived from small RNA-Seq data. Bioinformatics. 2013;29(20):2651–2.PubMedCrossRef
132.
Sánchez-Tilló E, et al. β-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc Natl Acad Sci. 2011;108(48):19204–9.PubMedPubMedCentralCrossRef
133.
Sánchez-Tilló E, et al. ZEB1 and TCF4 reciprocally modulate their transcriptional activities to regulate Wnt target gene expression. Oncogene. 2015;34(46):5760–70.
134.
Wang J, et al. Next generation sequencing of pancreatic cyst fluid microRNAs from low grade-benign and high grade-invasive lesions. Cancer Lett. 2015;356(2):404–9.PubMedCrossRef
135.
Yang J-H. et al. deepBase: a database for deeply annotating and mining deep sequencing data. Nucleic Acids Res. 2010;38:123–130.
136.
Alexiou P, et al. miRGen 2.0: a database of microRNA genomic information and regulation. Nucleic acids Res. 2010;38:137–141.
137.
Griffiths-Jones S, et al. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36 suppl 1:D154–8.PubMed
138.
Wang W-C, et al. miRExpress: analyzing high-throughput sequencing data for profiling microRNA expression. BMC Bioinformatics. 2009;10(1):1.CrossRef
139.
Maragkakis M, et al. CLIPSeqTools—a novel bioinformatics CLIP-seq analysis suite. RNA. 2016;22(1):1–9.
140.
Vishnubalaji R, et al. Genome-wide mRNA and miRNA expression profiling reveal multiple regulatory networks in colorectal cancer. Cell Death Dis. 2015;6(1):e1614.PubMedPubMedCentralCrossRef
141.
Zhu L, et al. miR-34a screened by miRNA profiling negatively regulates Wnt/β-catenin signaling pathway in Aflatoxin B1 induced hepatotoxicity. Sci Rep. 2015;5(16732):1–13.
142.
Murugavel K, et al. Prevalence of aflatoxin B1 in liver biopsies of proven hepatocellular carcinoma in India determined by an in-house immunoperoxidase test. J Med Microbiol. 2007;56(11):1455–9.PubMedCrossRef
143.
Wu H-C, et al. Aflatoxin B1 exposure, hepatitis B virus infection, and hepatocellular carcinoma in Taiwan. Cancer Epidemiol Biomark Prev. 2009;18(3):846–53.CrossRef
144.
Hamid AS, et al. Aflatoxin B1-induced hepatocellular carcinoma in developing countries: Geographical distribution, mechanism of action and prevention (Review). Oncol Lett. 2013;5(4):1087–92.PubMedPubMedCentral
145.
Chen W-Y, et al. MicroRNA-34a regulates WNT/TCF7 signaling and inhibits bone metastasis in Ras-activated prostate cancer. Oncotarget. 2015;6(1):441.PubMed
146.
147.
Morin RD, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res. 2008;18(4):610–21.PubMedPubMedCentralCrossRef
148.
149.
150.
151.
Wu C, et al. ToppMiR: ranking microRNAs and their mRNA targets based on biological functions and context. Nucleic Acids Res. 2014;42:107–113.
152.
Cho S, et al. MiRGator v3. 0: a microRNA portal for deep sequencing, expression profiling and mRNA targeting. Nucleic Acids Res. 2013;41(D1):D252–7.PubMedCrossRef
153.
Bonet F, et al. MiR‐23b and miR‐199a impair epithelial‐to‐mesenchymal transition during atrioventricular endocardial cushion formation. Dev Dyn. 2015;244(10):1259–75.PubMedCrossRef
154.
Duan Z, et al. MicroRNA-199a-3p is downregulated in human osteosarcoma and regulates cell proliferation and migration. Mol Cancer Ther. 2011;10(8):1337–45.PubMedPubMedCentralCrossRef
155.
Friedersdorf MB, Keene JD. Advancing the functional utility of PAR-CLIP by quantifying background binding to mRNAs and lncRNAs. Genome Biol. 2014;15(1):1.CrossRef
156.
Zhang Y, et al. CLIP: viewing the RNA world from an RNA-protein interactome perspective. Sci China Life Sci. 2015;58(1):75–88.PubMedCrossRef
157.
158.
Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods. 2007;4(9):721–726.PubMedCrossRef
159.
Chang H, et al. CRISPR/cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Sci Rep. 2016;6(22312):1–12.
160.
161.
162.
Su J, et al. MicroRNA-200a suppresses the Wnt/β-catenin signaling pathway by interacting with β-catenin. Int J Oncol. 2012;40(4):1162–70.PubMed
163.
164.
Isobe T, et al. miR-142 regulates the tumorigenicity of human breast cancer stem cells through the canonical WNT signaling pathway. Elife. 2014;3:e01977.PubMedCentralCrossRef
165.
Vorvis C. et al. Transcriptomic and CRISPR/Cas9 technologies reveal FOXA2 as a tumor suppressor gene in pancreatic cancer. Am J Physiol Gastrointest Liver Physiol. 2016;ajpgi. 00035.2016.
166.
Alexander M, et al. MicroRNA-199a is induced in dystrophic muscle and affects WNT signaling, cell proliferation, and myogenic differentiation. Cell Death Differ. 2013;20(9):1194–208.PubMedPubMedCentralCrossRef
167.
168.
169.
Gao Y, Zhao Y. Self‐processing of ribozyme‐flanked RNAs into guide RNAs in vitro and in vivo for CRISPR‐mediated genome editing. J Integr Plant Biol. 2014;56(4):343–9.PubMedCrossRef
170.
171.
Zhang F, Wen Y, Guo X. CRISPR/Cas9 for genome editing: progress, implications and challenges. Hum Mol Genet. 2014;23(R1):R40–6.
172.
173.
DuPage M, Dooley AL, Jacks T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat Protoc. 2009;4(7):1064–72.PubMedPubMedCentralCrossRef
174.
Maddison K, Clarke AR. New approaches for modelling cancer mechanisms in the mouse. J Pathol. 2005;205(2):181–93.PubMedCrossRef
175.
Babaei-Jadidi R, et al. FBXW7 influences murine intestinal homeostasis and cancer, targeting Notch, Jun, and DEK for degradation. J Exp Med. 2011;208(2):295–312.PubMedPubMedCentralCrossRef
176.
Attardi LD, Donehower LA. Probing p53 biological functions through the use of genetically engineered mouse models. Mutat Res. 2005;576(1):4–21.PubMedCrossRef
177.
178.
179.
Takahashi Y, et al. MicroRNA-184 modulates canonical Wnt signaling through the regulation of frizzled-7 expression in the retina with ischemia-induced neovascularization. FEBS Lett. 2015;589(10):1143–9.PubMedPubMedCentralCrossRef
180.
Scott A, Fruttiger M. Oxygen-induced retinopathy: a model for vascular pathology in the retina. Eye. 2010;24(3):416–21.PubMedCrossRef
181.
Stahl, A., et al., The Mouse Model of Oxygen-Induced Retinopathy (OIR), in The Textbook of Angiogenesis and Lymphangiogenesis: Methods and Applications. 2012, Springer. p. 181–188.
182.
Ventura A, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 ∼ 92 family of miRNA clusters. Cell. 2008;132(5):875–86.PubMedPubMedCentralCrossRef
183.
Landskroner-Eiger S, et al. Endothelial miR-17 ∼ 92 cluster negatively regulates arteriogenesis via miRNA-19 repression of WNT signaling. Proc Natl Acad Sci. 2015;112(41):12812–7.PubMedPubMedCentralCrossRef
184.
Cai W-Y, et al. The Wnt–β-catenin pathway represses let-7 microRNA expression through transactivation of Lin28 to augment breast cancer stem cell expansion. J Cell Sci. 2013;126(13):2877–89.PubMedCrossRef
185.
Hynds RE, Giangreco A. Concise review: the relevance of human stem cell‐derived organoid models for epithelial translational medicine. Stem Cells. 2013;31(3):417–22.PubMedPubMedCentralCrossRef
186.
Sato T, Clevers H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science. 2013;340(6137):1190–4.PubMedCrossRef
187.
Katano T, et al. Establishment of a long-term three-dimensional primary culture of mouse glandular stomach epithelial cells within the stem cell niche. Biochem Biophys Res Commun. 2013;432(4):558–63.PubMedCrossRef
188.
189.
Lorenzi F, et al. Fbxw7-associated drug resistance is reversed by induction of terminal differentiation in murine intestinal organoid culture. Mol Ther Methods Clin Dev. 2016;3:16024.PubMedPubMedCentralCrossRef
190.
Pylayeva-Gupta Y, Lee KE, Bar-Sagi D. Microdissection and culture of murine pancreatic ductal epithelial cells. Pancreat Cancer: Methods Protoc. 2013;267–279
191.
Jin L, et al. Colony-forming cells in the adult mouse pancreas are expandable in Matrigel and form endocrine/acinar colonies in laminin hydrogel. Proc Natl Acad Sci. 2013;110(10):3907–12.PubMedPubMedCentralCrossRef
192.
Huch M, et al. Unlimited in vitro expansion of adult bi‐potent pancreas progenitors through the Lgr5/R‐spondin axis. EMBO J. 2013;32(20):2708–21.PubMedPubMedCentralCrossRef
193.
194.
Network CGA. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487(7407):330–7.CrossRef
195.
Schwickert A, et al. microRNA miR-142-3p Inhibits Breast Cancer Cell Invasiveness by Synchronous Targeting of WASL, Integrin Alpha V, and Additional Cytoskeletal Elements. PloS One. 2015;10(12)
196.
Cao XC, et al. miR‐142‐3p inhibits cancer cell proliferation by targeting CDC25C. Cell Prolif. 2016;49(1):58–68.PubMedCrossRef
197.
Lustig B, et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol. 2002;22(4):1184–93.PubMedPubMedCentralCrossRef
198.
199.
Shamir ER, Ewald AJ. Three-dimensional organotypic culture: experimental models of mammalian biology and disease. Nat Rev Mol Cell Biol. 2014;15(10):647–64.PubMedPubMedCentralCrossRef
200.
Fatehullah A, Tan SH, Barker N. Organoids as an in vitro model of human development and disease. Nat Cell Biol. 2016;18(3):246–54.PubMedCrossRef
201.
202.
Fang Z, Cui X. Design and validation issues in RNA-seq experiments. Brief Bioinform. 2011;12(3):280–7.
203.
204.
Takasato M, et al. Directing human embryonic stem cell differentiation towards a renal lineage generates a self-organizing kidney. Nat Cell Biol. 2014;16(1):118–26.PubMedCrossRef
205.
Briggs JA, et al. Integration‐free induced pluripotent stem cells model genetic and neural developmental features of down syndrome etiology. Stem Cells. 2013;31(3):467–78.PubMedCrossRef
206.
Ankala A, Hegde M. Genomic technologies and the new era of genomic medicine. J Mol Diagn. 2014;16(1):7–10.PubMedCrossRef
207.
Cottrell CE, et al. Validation of a next-generation sequencing assay for clinical molecular oncology. J Mol Diagn. 2014;16(1):89–105.PubMedCrossRef
208.
Gargis AS, et al. Assuring the quality of next-generation sequencing in clinical laboratory practice. Nat Biotechnol. 2012;30(11):1033–6.PubMedCrossRef
209.
Ciani L, Salinas PC. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci. 2005;6(5):351–62.PubMedCrossRef
210.
211.
Konig J, et al. iCLIP-Transcriptome-wide Mapping of Protein-RNA Interactions with individual nucleotide resolution. J Vis Exp. 2011;(50):1–7.
212.
Friedländer MR, et al. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol. 2008;26(4):407–15.PubMedCrossRef
213.
Hünten S, et al. The p53/microRNA network in cancer: experimental and bioinformatics approaches, in MicroRNA Cancer Regulation. Springer. 2013;77–101.
214.
Ji S. et al., miR-574-5p negatively regulates Qki6/7 to impact β-catenin/Wnt signalling and the development of colorectal cancer. Gut. 2012;gutjnl-2011-301083.
215.
Zhang N, et al. microRNA-7 is a novel inhibitor of YY1 contributing to colorectal tumorigenesis. Oncogene. 2013;32(42):5078–88.PubMedCrossRef
216.
217.
Subramanian M, et al. MiR‐29b Downregulates Canonical Wnt Signaling by Suppressing Coactivators of β‐Catenin in Human Colorectal Cancer Cells. J Cell Biochem. 2014;115(11):1974–84.PubMed
218.
Shen G, et al. miR-106b downregulates adenomatous polyposis coli and promotes cell proliferation in human hepatocellular carcinoma. Carcinogenesis. 2013;34(1):211–9.PubMedCrossRef
219.
Zhang Y, et al. Hepatitis C virus‐induced up‐regulation of microRNA‐155 promotes hepatocarcinogenesis by activating Wnt signaling. Hepatology. 2012;56(5):1631–40.PubMedCrossRef
220.
Xu J, et al. MicroRNA‐122 suppresses cell proliferation and induces cell apoptosis in hepatocellular carcinoma by directly targeting Wnt/β‐catenin pathway. Liver Int. 2012;32(5):752–60.PubMedCrossRef
221.
Zhang J-G, et al. MiR-148b suppresses cell proliferation and invasion in hepatocellular carcinoma by targeting WNT1/β-catenin pathway. Sci Rep. 2015;5(8087):1–9.
222.
Gu W, Li X, Wang J. miR-139 regulates the proliferation and invasion of hepatocellular carcinoma through the WNT/TCF-4 pathway. Oncol Rep. 2014;31(1):397–404.PubMed
223.
Valastyan S, Weinberg RA. miR-31: a crucial overseer of tumor metastasis and other emerging roles. Cell Cycle. 2010;9(11):2124–9.PubMedCrossRef
224.
Kim S-J, et al. Development of microRNA-145 for therapeutic application in breast cancer. J Control Release. 2011;155(3):427–34.PubMedCrossRef
225.
Hsieh I-S, et al. MicroRNA-320 suppresses the stem cell-like characteristics of prostate cancer cells by down-regulating the Wnt/beta-catenin signaling pathway. Carcinogenesis. 2013;34(3):530–538.
226.
Xu W, et al. MicroRNA‐191, by promoting the EMT and increasing CSC‐like properties, is involved in neoplastic and metastatic properties of transformed human bronchial epithelial cells. Mol Carcinog. 2015;54(S1)
227.
Deng X, et al. MiR-146b-5p promotes metastasis and induces epithelial-mesenchymal transition in thyroid cancer by targeting ZNRF3. Cell Physiol Biochem. 2015;35(1):71–82.PubMedCrossRef
228.
Parikh A, et al. microRNA-181a has a critical role in ovarian cancer progression through the regulation of the epithelial–mesenchymal transition. Nat Commun. 2014;5(2977):1–16.
229.
Jia Y, et al. Inhibition of SOX17 by microRNA 141 and methylation activates the WNT signaling pathway in esophageal cancer. J Mol Diagn. 2012;14(6):577–85.PubMedCrossRef
Metadata
Title
Wnt-signalling pathways and microRNAs network in carcinogenesis: experimental and bioinformatics approaches
Authors
Emenike K. Onyido
Eloise Sweeney
Abdolrahman Shams Nateri
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2016
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-016-0541-3

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