microRNA signature for human pancreatic cancer invasion and metastasis (Review)
- Authors:
- He Cheng
- Si Shi
- Xiaochen Cai
- Jiang Long
- Jin Xu
- Chen Liu
- Xianjun Yu
-
Affiliations: Department of Pancreatic and Hepatobiliary Surgery, Fudan University, Shanghai Cancer Center, Shanghai 200032, P.R. China , Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, P.R. China - Published online on: May 21, 2012 https://doi.org/10.3892/etm.2012.585
- Pages: 181-187
This article is mentioned in:
Abstract
Jemal A, Siegel R, Xu J and Ward E: Cancer statistics, 2010. CA Cancer J Clin. 60:277–300. 2010. View Article : Google Scholar | |
Zuckerman DS and Ryan DP: Adjuvant therapy for pancreatic cancer: a review. Cancer. 112:243–249. 2008. View Article : Google Scholar : PubMed/NCBI | |
Esquela-Kerscher A and Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006. View Article : Google Scholar | |
Denli AM, Tops BB, Plasterk RH, Ketting RF and Hannon GJ: Processing of primary microRNAs by the microprocessor complex. Nature. 432:231–235. 2004. View Article : Google Scholar : PubMed/NCBI | |
Wightman B, Ha I and Ruvkun G: Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 75:855–862. 1993. View Article : Google Scholar : PubMed/NCBI | |
Reinhart BJ, Slack FJ, Basson M, et al: The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 403:901–906. 2000. View Article : Google Scholar : PubMed/NCBI | |
Calin GA, Dumitru CD, Shimizu M, et al: Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA. 99:15524–15529. 2002. View Article : Google Scholar : PubMed/NCBI | |
Bloomston M, Frankel WL, Petrocca F, et al: microRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA. 229:1901–1908. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lee JW, Choi CH, Choi JJ, et al: Altered microRNA expression in cervical carcinomas. Clin Cancer Res. 14:2535–2542. 2008. View Article : Google Scholar : PubMed/NCBI | |
Iorio MV, Ferracin M, Liu CG, et al: MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65:7065–7070. 2005. View Article : Google Scholar : PubMed/NCBI | |
Budhu A, Jia HL, Forgues M, et al: Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology. 47:897–907. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ma L, Teruya-Feldstein J and Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 449:682–688. 2007. View Article : Google Scholar : PubMed/NCBI | |
Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST and Patel T: MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 133:647–658. 2007. View Article : Google Scholar : PubMed/NCBI | |
Asangani IA, Rasheed SA, Nikolova DA, et al: MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene. 27:2128–2136. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lin SL, Chiang A, Chang D and Ying SY: Loss of mir-146a function in hormone-refractory prostate cancer. RNA. 14:417–424. 2008. View Article : Google Scholar : PubMed/NCBI | |
Crawford M, Brawner E, Batte K, et al: MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochem Biophys Res Commun. 373:607–612. 2008. View Article : Google Scholar : PubMed/NCBI | |
Huang Q, Gumireddy K, Schrier M, et al: The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol. 10:202–210. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hwang JH, Voortman J, Giovannetti E, et al: Identification of microRNA-21 as a biomarker for chemoresistance and clinical outcome following adjuvant therapy in resectable pancreatic cancer. PloS One. 5:e106302010. View Article : Google Scholar : PubMed/NCBI | |
Giovannetti E, Funel N, Peters GJ, et al: MicroRNA-21 in pancreatic cancer: correlation with clinical outcome and pharmacologic aspects underlying its role in the modulation of gemcitabine activity. Cancer Res. 70:4528–4538. 2010. View Article : Google Scholar : PubMed/NCBI | |
Moriyama T, Ohuchida K, Mizumoto K, et al: MicroRNA-21 modulates biological functions of pancreatic cancer cells including their proliferation, invasion, and chemoresistance. Mol Cancer Ther. 8:1067–1074. 2009. View Article : Google Scholar | |
Bhaumik D, Scott GK, Schokrpur S, Patil CK, Campisi J and Benz CC: Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene. 27:5643–5647. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kogo R, Mimori K, Tanaka F, Komune S and Mori M: Clinical significance of miR-146a in gastric cancer cases. Clin Cancer Res. 17:4277–4284. 2011. View Article : Google Scholar : PubMed/NCBI | |
Fujioka S, Sclabas GM, Schmidt C, et al: Function of nuclear factor kappaB in pancreatic cancer metastasis. Clin Cancer Res. 9:346–354. 2003.PubMed/NCBI | |
Karin M: Nuclear factor-kappaB in cancer development and progression. Nature. 441:431–436. 2006. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Vandenboom TG II, Wang Z, et al: miR-146a suppresses invasion of pancreatic cancer cells. Cancer Res. 70:1486–1495. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lin F, Wang X, Jie Z, et al: Inhibitory effects of miR-146b-5p on cell migration and invasion of pancreatic cancer by targeting MMP16. J Huazhong Univ Sci Technolog Med Sci. 31:509–514. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ma Y, Yu S, Zhao W, Lu Z and Chen J: miR-27a regulates the growth, colony formation and migration of pancreatic cancer cells by targeting Sprouty2. Cancer Lett. 298:150–158. 2010. View Article : Google Scholar : PubMed/NCBI | |
Yu J, Ohuchida K, Mizumoto K, et al: MicroRNA, hsa-miR-200c, is an independent prognostic factor in pancreatic cancer and its upregulation inhibits pancreatic cancer invasion but increases cell proliferation. Mol Cancer. 9:1692010. View Article : Google Scholar : PubMed/NCBI | |
Wang F, Xue X, Wei J, et al: hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations. Br J Cancer. 103:567–574. 2010. View Article : Google Scholar : PubMed/NCBI | |
Preis M, Gardner TB, Gordon SR, et al: MicroRNA-10b expression correlates with response to neoadjuvant therapy and survival in pancreatic ductal adenocarcinoma. Clin Cancer Res. 17:5812–5821. 2011. View Article : Google Scholar : PubMed/NCBI | |
Srivastava SK, Bhardwaj A, Singh S, et al: MicroRNA-150 directly targets MUC4 and suppresses growth and malignant behavior of pancreatic cancer cells. Carcinogenesis. 32:1832–1839. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yu J, Ohuchida K, Mizumoto K, Fujita H, Nakata K and Tanaka M: MicroRNA miR-17-5p is overexpressed in pancreatic cancer, associated with a poor prognosis, and involved in cancer cell proliferation and invasion. Cancer Biol Ther. 10:748–757. 2010. View Article : Google Scholar : PubMed/NCBI | |
Muniyappa MK, Dowling P, Henry M, et al: MiRNA-29a regulates the expression of numerous proteins and reduces the invasiveness and proliferation of human carcinoma cell lines. Eur J Cancer. 45:3104–3118. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yan H, Wu J, Liu W, et al: MicroRNA-20a overexpression inhibited proliferation and metastasis of pancreatic carcinoma cells. Hum Gene Ther. 21:1723–1734. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hamada S, Satoh K, Fujibuchi W, et al: MiR-126 acts as a tumor suppressor in pancreatic cancer cells via the regulation of ADAM9. Mol Cancer Res. 10:3–10. 2012. View Article : Google Scholar : PubMed/NCBI | |
Li W, Yuan Y, Huang L, Qiao M and Zhang Y: Metformin alters the expression profiles of microRNAs in human pancreatic cancer cells. Diabetes Res Clin Pract. 96:187–195. 2012. View Article : Google Scholar : PubMed/NCBI | |
Thiery JP, Acloque H, Huang RY and Nieto MA: Epithelialmesenchymal transitions in development and disease. Cell. 139:871–890. 2009. View Article : Google Scholar : PubMed/NCBI | |
Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 7:131–142. 2006. View Article : Google Scholar : PubMed/NCBI | |
Christiansen JJ and Rajasekaran AK: Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 66:8319–8326. 2006. View Article : Google Scholar : PubMed/NCBI | |
Xiong H, Hong J, Du W, et al: Roles of STAT3 and ZEB1 proteins in E-cadherin down-regulation and human colorectal cancer epithelial-mesenchymal transition. J Biol Chem. 287:5819–5832. 2012. View Article : Google Scholar : PubMed/NCBI | |
Maier HJ, Schmidt-Strassburger U, Huber MA, Wiedemann EM, Beug H and Wirth T: NF-kappaB promotes epithelialmesenchymal transition, migration and invasion of pancreatic carcinoma cells. Cancer Lett. 295:214–228. 2010. View Article : Google Scholar : PubMed/NCBI | |
Spaderna S, Schmalhofer O, Wahlbuhl M, et al: The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 68:537–544. 2008. View Article : Google Scholar : PubMed/NCBI | |
Korpal M, Lee ES, Hu G and Kang Y: The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem. 283:14910–14914. 2008. View Article : Google Scholar : PubMed/NCBI | |
Burk U, Schubert J, Wellner U, et al: A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9:582–589. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wellner U, Schubert J, Burk UC, et al: The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 11:1487–1495. 2009. View Article : Google Scholar : PubMed/NCBI | |
Torrisani J, Bournet B, du Rieu MC, et al: let-7 microRNA transfer in pancreatic cancer-derived cells inhibits in vitro cell proliferation but fails to alter tumor progression. Hum Gene Ther. 20:831–844. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ali S, Almhanna K, Chen W, Philip PA and Sarkar FH: Differentially expressed miRNAs in the plasma may provide a molecular signature for aggressive pancreatic cancer. Am J Transl Res. 3:28–47. 2010.PubMed/NCBI | |
Li Y, VandenBoom TG II, Kong D, et al: Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res. 69:6704–6712. 2009. View Article : Google Scholar : PubMed/NCBI | |
Wicha MS, Liu S and Dontu G: Cancer stem cells: an old idea - a paradigm shift. Cancer Res. 66:1883–1890; discussion. 1895–1896. 2006. View Article : Google Scholar : PubMed/NCBI | |
Bonnet D and Dick JE: Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 3:730–737. 1997. View Article : Google Scholar : PubMed/NCBI | |
Singh SK, Hawkins C, Clarke ID, et al: Identification of human brain tumour initiating cells. Nature. 432:396–401. 2004. View Article : Google Scholar : PubMed/NCBI | |
Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Scie USA. 100:3983–3988. 2003. View Article : Google Scholar : PubMed/NCBI | |
O’Brien CA, Pollett A, Gallinger S and Dick JE: A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 445:106–110. 2007.PubMed/NCBI | |
Li C, Heidt DG, Dalerba P, et al: Identification of pancreatic cancer stem cells. Cancer Res. 67:1030–1037. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hermann PC, Huber SL, Herrler T, et al: Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 1:313–323. 2007. View Article : Google Scholar | |
Moriyama T, Ohuchida K, Mizumoto K, et al: Enhanced cell migration and invasion of CD133+ pancreatic cancer cells cocultured with pancreatic stromal cells. Cancer. 116:3357–3368. 2010. View Article : Google Scholar : PubMed/NCBI | |
May R, Sureban SM, Lightfoot SA, et al: Identification of a novel putative pancreatic stem/progenitor cell marker DCAMKL-1 in normal mouse pancreas. Am J Physiol Gastrointest Liver Physiol. 299:G303–310. 2010. View Article : Google Scholar : PubMed/NCBI | |
Sureban SM, May R, Lightfoot SA, et al: DCAMKL-1 regulates epithelial-mesenchymal transition in human pancreatic cells through a miR-200a-dependent mechanism. Cancer Res. 71:2328–2338. 2011. View Article : Google Scholar : PubMed/NCBI | |
Tarasov V, Jung P, Verdoodt B, et al: Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle. 6:1586–1593. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bommer GT, Gerin I, Feng Y, et al: p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol. 17:1298–1307. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ji Q, Hao X, Zhang M, et al: MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PloS One. 4:e68162009. View Article : Google Scholar : PubMed/NCBI | |
Ji Q, Hao X, Meng Y, et al: Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer. 8:2662008. View Article : Google Scholar : PubMed/NCBI | |
Bao B, Ali S, Banerjee S, et al: Curcumin analogue CDF inhibits pancreatic tumor growth by switching on suppressor microRNAs and attenuating EZH2 expression. Cancer Res. 72:335–345. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Li Y, Banerjee S and Sarkar FH: Emerging role of Notch in stem cells and cancer. Cancer Lett. 279:8–12. 2009. View Article : Google Scholar : PubMed/NCBI | |
Demarest RM, Ratti F and Capobianco AJ: It’s T-ALL about Notch. Oncogene. 27:5082–5091. 2008. | |
Dotto GP: Notch tumor suppressor function. Oncogene. 27:5115–5123. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Banerjee S, Li Y, Rahman KM, Zhang Y and Sarkar FH: Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res. 66:2778–2784. 2006. View Article : Google Scholar | |
Strizzi L, Hardy KM, Seftor EA, et al: Development and cancer: at the crossroads of Nodal and Notch signaling. Cancer Res. 69:7131–7134. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ristorcelli E and Lombardo D: Targeting Notch signaling in pancreatic cancer. Expert Opin Ther Targets. 14:541–552. 2010. View Article : Google Scholar : PubMed/NCBI | |
Nalls D, Tang SN, Rodova M, Srivastava RK and Shankar S: Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PloS One. 6:e240992011. View Article : Google Scholar : PubMed/NCBI | |
Bao B, Wang Z, Ali S, et al: Notch-1 induces epithelial-mesenchymal transition consistent with cancer stem cell phenotype in pancreatic cancer cells. Cancer Lett. 307:26–36. 2011. View Article : Google Scholar : PubMed/NCBI | |
Matthaios D, Zarogoulidis P, Balgouranidou I, Chatzaki E and Kakolyris S: Molecular pathogenesis of pancreatic cancer and clinical perspectives. Oncology. 81:259–272. 2011. View Article : Google Scholar : PubMed/NCBI | |
Feldmann G, Dhara S, Fendrich V, et al: Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res. 67:2187–2196. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ferretti E, De Smaele E, Miele E, et al: Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 27:2616–2627. 2008. View Article : Google Scholar : PubMed/NCBI | |
Northcott PA, Fernandez LA, Hagan JP, et al: The miR-17/92 polycistron is up-regulated in sonic hedgehog-driven medulloblastomas and induced by N-myc in sonic hedgehog-treated cerebellar neural precursors. Cancer Res. 69:3249–3255. 2009. View Article : Google Scholar : PubMed/NCBI | |
Friggi-Grelin F, Lavenant-Staccini L and Therond P: Control of antagonistic components of the hedgehog signaling pathway by microRNAs in Drosophila. Genetics. 179:429–439. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tsuda N, Ishiyama S, Li Y, Ioannides CG, Abbruzzese JL and Chang DZ: Synthetic microRNA designed to target glioma-associated antigen 1 transcription factor inhibits division and induces late apoptosis in pancreatic tumor cells. Clin Cancer Res. 12:6557–6564. 2006. View Article : Google Scholar | |
Yu S, Lu Z, Liu C, et al: miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Res. 70:6015–6025. 2010. View Article : Google Scholar : PubMed/NCBI | |
Vogt M, Munding J, Gruner M, et al: Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch. 458:313–322. 2011. View Article : Google Scholar : PubMed/NCBI | |
Tashiro E, Tsuchiya A and Imoto M: Functions of cyclin D1 as an oncogene and regulation of cyclin D1 expression. Cancer Sci. 98:629–635. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lee KH, Lotterman C, Karikari C, et al: Epigenetic silencing of MicroRNA miR-107 regulates cyclin-dependent kinase 6 expression in pancreatic cancer. Pancreatology. 9:293–301. 2009. View Article : Google Scholar : PubMed/NCBI | |
Grewal IS and Flavell RA: CD40 and CD154 in cell-mediated immunity. Annu Rev Immunol. 16:111–135. 1998. View Article : Google Scholar : PubMed/NCBI | |
Costello RT, Gastaut JA and Olive D: What is the real role of CD40 in cancer immunotherapy? Immunology Today. 20:488–493. 1999. View Article : Google Scholar : PubMed/NCBI | |
Mees ST, Mardin WA, Sielker S, et al: Involvement of CD40 targeting miR-224 and miR-486 on the progression of pancreatic ductal adenocarcinomas. Ann Surg Oncol. 16:2339–2350. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kouzarides T: Histone acetylases and deacetylases in cell proliferation. Curr Opin Genet Dev. 9:40–48. 1999. View Article : Google Scholar | |
Ida K, Kitabayashi I, Taki T, et al: Adenoviral E1A-associated protein p300 is involved in acute myeloid leukemia with t(11;22) (q23;q13). Blood. 90:4699–4704. 1997.PubMed/NCBI | |
Mees ST, Mardin WA, Wendel C, et al: EP300 - a miRNA-regulated metastasis suppressor gene in ductal adenocarcinomas of the pancreas. Int J Cancer. 126:114–124. 2010. View Article : Google Scholar : PubMed/NCBI |