Hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations

British Journal of Cancer

Volumn 103, Issue 4, 2010, Pages 567-574

  Wang, F ^a   Xue, X ^a   Wei, J ^a   An, Y ^a   Yao, J ^a,b   Cai, H ^a   Wu, J ^a   Dai, C ^a   Qian, Z ^a   Xu, Z ^a   Miao, Y ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b YANGZHOU UNIVERSITY   (China)

Author keywords

ABCG2; invasion; migration; miRNA; side population cells

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; HSA MIR 520H; MESSENGER RNA; MICRORNA; OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GENE THERAPY; CANCER INHIBITION; CELL CYCLE PROGRESSION; CELL INVASION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; PANCREATIC NEOPLASMS;

EID: 77955517749     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605724     Document Type: Article

References (79)

1. Agirre X, Vilas-Zornoza A, Jiménez-Velasco A, Martin-Subero JI, Cordeu L, Gárate L, San José-Eneriz E, Abizanda G, Rodŕguez-Otero P, Fortes P, Rifón J, Bandrés E, Calasanz MJ, Mart́n V, Heiniger A, Torres A, Siebert R, Román-Gomez J, Prósper F (2009) Epigenetic silencing of the tumor suppressor microRNA Hsa-miR-124a regulates CDK6 expression and confers a poor prognosis in acute lymphoblastic leukemia. Cancer Res 69: 4443-4453
2. Aguda BD, Kim Y, Piper-Hunter MG, Friedman A, Marsh CB (2008) MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci USA 105: 19678-19683
3. Aqeilan RI, Calin GA, Croce CM (2010) miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ 17: 215-220
4. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S, Allgayer H (2008) MicroRNA-21 (miR-21) post-transcriptionally down-regulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27: 2128-2136
5. Bandi N, Zbinden S, Gugger M, Arnold M, Kocher V, Hasan L, Kappeler A, Brunner T, Vassella E (2009) miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res 69: 5553-5559
6. Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, Rossi S, Calin GA, Mukherjee P (2009) MiR-15a and MiR-16 Control Bmi-1 Expression in Ovarian Cancer. Cancer Res 69: 9090-9095
7. Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, D'Urso L, Pagliuca A, Biffoni M, Labbaye C, Bartucci M, Muto G, Peschle C, De Maria R (2008) The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 14: 1271-1277
8. Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, Chou SH, Chien CS, Ku HH, Lo JF (2008) Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res 14: 4085-4095
9. Coulouarn C, Factor VM, Andersen JB, Durkin ME, Thorgeirsson SS (2009) Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene 28: 3526-3536
10. Cowden Dahl KD, Dahl R, Kruichak JN, Hudson LG (2009) The epidermal growth factor receptor responsive miR-125a represses mesenchymal morphology in ovarian cancer cells. Neoplasia 11: 1208-1215
11. Dalmay T, Edwards DR (2006) MicroRNAs and the hallmarks of cancer. Oncogene 25: 6170-6175
12. Dou J, Wen P, Hu W, Li Y, Wu Y, Liu C, Zhao F, Hu K, Wang J, Jiang C, He X, Gu N (2009) Identifying tumor stem-like cells in mouse melanoma cell lines by analyzing the characteristics of side population cells. Cell Biol Int 33: 807-815
13. Doyle LA, Yang W, Abruzzo LE, Krogmann T, Gao Y, Rishi AK, Ross DD (1998) A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 95: 15665-15670
14. Evseenko DA, Paxton JW, Keelan JA (2007) Independent regulation of apical and basolateral drug transporter expression and function in placental trophoblasts by cytokines, steroids, and growth factors. Drug Metab Dispos 35: 595-601
15. Fetsch PA, Abati A, Litman T, Morisaki K, Honjo Y, Mittal K, Bates SE (2006) Localization of the ABCG2 mitoxantrone resistance-associated protein in normal tissues. Cancer Lett 235: 84-92
16. Fidler IJ (2003) The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 3: 453-458
17. Furuta M, Kozaki KI, Tanaka S, Arii S, Imoto I, Inazawa J (2009) miR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis 31(5): 766-776
18. Gandellini P, Folini M, Longoni N, Pennati M, Binda M, Colecchia M, Salvioni R, Supino R, Moretti R, Limonta P, Valdagni R, Daidone MG, Zaffaroni N (2009) miR-205 exerts tumor-suppressive functions in human prostate through down-regulation of protein kinase Cepsilon. Cancer Res 69: 2287-2295
19. Grady WM, Parkin RK, Mitchell PS, Lee JH, Kim YH, Tsuchiya KD, Washington MK, Paraskeva C, Willson JK, Kaz AM, Kroh EM, Allen A, Fritz BR, Markowitz SD, Tewari M (2008) Epigenetic silencing of the intronic microRNA hsa-miR-342 and its host gene EVL in colorectal cancer. Oncogene 27: 3880-3888
20. Guo J, Anderson MG, Tapang P, Palma JP, Rodriguez LE, Niquette A, Li J, Bouska JJ, Wang G, Semizarov D, Albert DH, Donawho CK, Glaser KB, Shah OJ (2009) Identification of genes that confer tumor cell resistance to the aurora B kinase inhibitor, AZD1152. Pharmacogenomics J 9: 90-102
21. Gupta GP, Massagué J (2006) Cancer metastasis: building a framework. Cell 127: 679-695
22. Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF, Mori M (2006) Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 24: 506-513
23. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK (2004) A distinct 'side population' of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 101: 14228-14233
24. Ho MM, Ng AV, Lam S, Hung JY (2007) Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 67: 4827-4833
25. Hoffman AE, Zheng T, Yi C, Leaderer D, Weidhaas J, Slack F, Zhang Y, Paranjape T, Zhu Y (2009) microRNA miR-196a-2 and breast cancer: a genetic and epigenetic association study and functional analysis. Cancer Res 69: 5970-5977
26. Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, Egan DA, Li A, Huang G, Klein-Szanto AJ, Gimotty PA, Katsaros D, Coukos G, Zhang L, Puré E, Agami R (2008) The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 10: 202-210
27. Hurst DR, Edmonds MD, Scott GK, Benz CC, Vaidya KS, Welch DR (2009) Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res 69: 1279-1283
28. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59: 225-249
29. Kim S, Lee UJ, Kim MN, Lee EJ, Kim JY, Lee MY, Choung S, Kim YJ, Choi YC (2008) MicroRNA miR-199a* regulates the MET proto-Oncogene and the downstream extracellular signal-regulated kinase 2 (ERK2). J Biol Chem 283: 18158-18166
30. König J, Hartel M, Nies AT, Martignoni ME, Guo J, Büchler MW, Friess H, Keppler D (2005) Expression and localization of human multidrug resistance protein (ABCC) family members in pancreatic carcinoma. Int J Cancer 115: 359-367
31. Korpal M, Lee ES, Hu G, Kang Y (2008) 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
32. Le Sage C, Nagel R, Egan DA, Schrier M, Mesman E, Mangiola A, Anile C, Maira G, Mercatelli N, Ciafrè SA, Farace MG, Agami R (2007) Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 26: 3699-3708
33. Lee KH, Chen YL, Yeh SD, Hsiao M, Lin JT, Goan YG, Lu PJ (2009) MicroRNA-330 acts as tumor suppressor and induces apoptosis of prostate cancer cells through E2F1-mediated suppression of Akt phosphorylation. Oncogene 28: 3360-3370
34. Li XF, Yan PJ, Shao ZM (2009) Downregulation of miR-193b contributes to enhance urokinase-type plasminogen activator (uPA) expression and tumor progression and invasion in human breast cancer. Oncogene 28: 3937-3948
35. Liao R, Sun J, Zhang L, Lou G, Chen M, Zhou D, Chen Z, Zhang S (2008) MicroRNAs play a role in the development of human hematopoietic stem cells. J Cell Biochem 104: 805-817
36. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773
37. Lin SL, Chiang A, Chang D, Ying SY (2008) Loss of mir-146a function in hormone-refractory prostate cancer. RNA 14: 417-424
38. Ma L, Teruya-Feldstein J, Weinberg RA (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688
39. Mohan A, Kandalam M, Ramkumar HL, Gopal L, Krishnakumar S (2006) Stem cell markers: ABCG2 and MCM2 expression in retinoblastoma. Br J Ophthalmol 90: 889-893
40. Musiyenko A, Bitko V, Barik S (2008) Ectopic expression of miR-126*, an intronic product of the vascular endothelial EGF-like 7 gene, regulates prostein translation and invasiveness of prostate cancer LNCaP cells. J Mol Med 86: 313-322
41. Nakanishi T, Bailey-Dell KJ, Hassel BA, Shiozawa K, Sullivan DM, Turner J, Ross DD (2006) Novel 5 untranslated region variants of BCRP mRNA are differentially expressed in drug-selected cancer cells and in normal human tissues: implications for drug resistance, tissue-specific expression, and alternative promoter usage. Cancer Res 66: 5007-5011
42. Noonan EJ, Place RF, Pookot D, Basak S, Whitson JM, Hirata H, Giardina C, Dahiya R (2009) miR-449a targets HDAC-1 and induces growth arrest in prostate cancer. Oncogene 28: 1714-1724
43. Okamoto A, Chikamatsu K, Sakakura K, Hatsushika K, Takahashi G, Masuyama K (2009) Expansion and characterization of cancer stem-like cells in squamous cell carcinoma of the head and neck. Oral Oncol 45: 633-639
44. Olempska M, Eisenach PA, Ammerpohl O, Ungefroren H, Fandrich F, Kalthoff H (2007) Detection of tumor stem cell markers in pancreatic carcinoma cell lines. Hepatobiliary Pancreat Dis Int 6: 92-97
45. Ostenfeld MS, Bramsen JB, Lamy P, Villadsen SB, Fristrup N, Sørensen KD, Ulhøi B, Borre M, Kjems J, Dyrskjøt L, Orntoft TF (2010) miR-145 induces caspase-dependent and-independent cell death in urothelial cancer cell lines with targeting of an expression signature present in Ta bladder tumors. Oncogene 29: 1073-1084
46. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG (2005) Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2-cancer cells are similarly tumorigenic. Cancer Res 65: 6207-6219
47. Pillai RS (2005) MicroRNA function: multiple mechanisms for a tiny RNA? RNA 11: 1753-1761
48. Qian B, Katsaros D, Lu L, Preti M, Durando A, Arisio R, Mu L, Yu H (2009) High miR-21 expression in breast cancer associated with poor disease-free survival in early stage disease and high TGF-beta1. Breast Cancer Res Treat 117: 131-140
49. Ribas J, Ni X, Haffner M, Wentzel EA, Salmasi AH, Chowdhury WH, Kudrolli TA, Yegnasubramanian S, Luo J, Rodriguez R, Mendell JT, Lupold SE (2009) miR-21: an androgen receptor-regulated microRNA that promotes hormone-dependent and hormone-independent prostate cancer growth. Cancer Res 69: 7165-7169
50. Sachdeva M, Zhu S, Wu F, Wu H, Walia V, Kumar S, Elble R, Watabe K, Mo YY (2009) p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci USA 106: 3207-3212
51. Saito Y, Suzuki H, Tsugawa H, Nakagawa I, Matsuzaki J, Kanai Y, Hibi T (2009) Chromatin remodeling at Alu repeats by epigenetic treatment activates silenced microRNA-512-5p with downregulation of Mcl-1 in human gastric cancer cells. Oncogene 28: 2738-2744
52. Seigel GM, Campbell LM, Narayan M, Gonzalez-Fernandez F (2005) Cancer stem cell characteristics in retinoblastoma. Mol Vis 11: 729-737
53. Sengupta S, den Boon JA, Chen IH, Newton MA, Stanhope SA, Cheng YJ, Chen CJ, Hildesheim A, Sugden B, Ahlquist P (2008) MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci USA 105: 5874-5878
54. Shi GM, Xu Y, Fan J, Zhou J, Yang XR, Qiu SJ, Liao Y, Wu WZ, Ji Y, Ke AW, Ding ZB, He YZ, Wu B, Yang GH, Qin WZ, Zhang W, Zhu J, Min ZH, Wu ZQ (2008) Identification of side population cells in human hepatocellular carcinoma cell lines with stepwise metastatic potentials. J Cancer Res Clin Oncol 134: 1155-1163
55. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY (2007) miR-21-mediated tumor growth. Oncogene 26: 2799-2803
56. Song B, Wang Y, Xi Y, Kudo K, Bruheim S, Botchkina GI, Gavin E, Wan Y, Formentini A, Kornmann M, Fodstad O, Ju J (2009) Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene 28: 4065-4074
57. Spizzo R, Nicoloso MS, Lupini L, Lu Y, Fogarty J, Rossi S, Zagatti B, Fabbri M, Veronese A, Liu X, Davuluri R, Croce CM, Mills G, Negrini M, Calin GA (2010) miR-145 participates with TP53 in a death-promoting regulatory loop and targets estrogen receptor-alpha in human breast cancer cells. Cell Death Differ 17: 246-254
58. Sung JM, Cho HJ, Yi H, Lee CH, Kim HS, Kim DK, Abd El-Aty AM, Kim JS, Landowski CP, Hediger MA, Shin HC (2008) Characterization of a stem cell population in lung cancer A549 cells. Biochem Biophys Res Commun 371: 163-167
59. Tavazoie SF, Alarcón C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massagué J (2008) Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451: 147-152
60. To KK, Polgar O, Huff LM, Morisaki K, Bates SE (2008a) Histone modifications at the ABCG2 promoter following treatment with histone deacetylase inhibitor mirror those in multidrug-resistant cells. Mol Cancer Res 6: 151-164
61. To KK, Zhan Z, Bates SE (2006) Aberrant promoter methylation of the ABCG2 gene in renal carcinoma. Mol Cell Biol 26: 8572-8585
62. To KK, Zhan Z, Litman T, Bates SE (2008b) Regulation of ABCG2 expression at the 3 untranslated region of its mRNA through modulation of transcript stability and protein translation by a putative microRNA in the S1 colon cancer cell line. Mol Cell Biol 28: 5147-5161
63. Tsang WP, Kwok TT (2009) The miR-18a* microRNA functions as a potential tumor suppressor by targeting on K-Ras. Carcinogenesis 30: 953-959
64. Turner JG, Gump JL, Zhang C, Cook JM, Marchion D, Hazlehurst L, Munster P, Schell MJ, Dalton WS, Sullivan DM (2006) ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood 108: 3881-3889
65. Veerla S, Lindgren D, Kvist A, Frigyesi A, Staaf J, Persson H, Liedberg F, Chebil G, Gudjonsson S, Borg A, Mansson W, Rovira C, Höglund M (2009) MiRNA expression in urothelial carcinomas: important roles of miR-10a, miR-222, miR-125b, miR-7 and miR-452 for tumor stage and metastasis, and frequent homozygous losses of miR-31. Int J Cancer 124: 2236-2242
66. Wang P, Zou F, Zhang X, Li H, Dulak A, Tomko Jr RJ, Lazo JS, Wang Z, Zhang L, Yu J (2009) microRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Res 69: 8157-8165
67. Wang Q, Li YC, Wang J, Kong J, Qi Y, Quigg RJ, Li X (2008) miR-17-92 cluster accelerates adipocyte differentiation by negatively regulating tumor-suppressor Rb2/p130. Proc Natl Acad Sci USA 105: 2889-2894
68. Wang X, Wang HK, McCoy JP, Banerjee NS, Rader JS, Broker TR, Meyers C, Chow LT, Zheng ZM (2009) Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6. RNA 15: 637-647
69. Wang YH, Li F, Luo B, Wang XH, Sun HC, Liu S, Cui YQ, Xu XX (2009) A side population of cells from a human pancreatic carcinoma cell line harbors cancer stem cell characteristics. Neoplasma 56: 371-378
70. Weigelt B, Peterse JL, van 't Veer LJ (2005) Breast cancer metastasis: markers and models. Nat Rev Cancer 5: 591-602
71. Weiss FU, Marques IJ, Woltering JM, Vlecken DH, Aghdassi A, Partecke LI, Heidecke CD, Lerch MM, Bagowski CP (2009) Retinoic acid receptor antagonists inhibit miR-10a expression and block metastatic behavior of pancreatic cancer. Gastroenterology 137: 2136-2145
72. Welch C, Chen Y, Stallings RL (2007) MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 26: 5017-5022
73. Wu H, Zhu S, Mo YY (2009) Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res 19: 439-448
74. Yajima T, Ochiai H, Uchiyama T, Takano N, Shibahara T, Azuma T (2009) Resistance to cytotoxic chemotherapy-induced apoptosis in side population cells of human oral squamous cell carcinoma cell line Ho-1-N-1. Int J Oncol 35: 273-280
75. Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL, Zeng YX, Shao JY (2008) MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 14: 2348-2360
76. Yin L, Castagnino P, Assoian RK (2008) ABCG2 expression and side population abundance regulated by a transforming growth factor beta-directed epithelial-mesenchymal transition. Cancer Res 68: 800-807
77. Zamore PD, Haley B (2005) Ribo-gnome: the big world of small RNAs. Science 309: 1519-1524
78. Zhang Z, Li Z, Gao C, Chen P, Chen J, Liu W, Xiao S, Lu H (2008) miR-21 plays a pivotal role in gastric cancer pathogenesis and progression. Lab Invest 88: 1358-1366
79. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY (2008) MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18: 350-359