Elevated microRNA-23a expression enhances the chemoresistance of colorectal cancer cells with microsatellite instability to 5-fluorouracil by directly targeting ABCF1

Current Protein and Peptide Science

Volumn 16, Issue 4, 2015, Pages 301-309

  Li, Xiang ^a   Li, Xiaolei ^a   Liao, Daixiang ^b   Wang, Xiaohui ^a   Wu, Zhiqiang ^a   Nie, Jing ^a   Bai, Miaomiao ^a   Fu, Xiaobing ^a   Mei, Qian ^a   Han, Weidong ^a  

^a CHINESE PLA GENERAL HOSPITAL   (China)

^b Mentougou District Hospital   (China)

Author keywords

5 fluorouracil (5 FU); ABCF1; Chemoresistance; CRCs; Microsatellite instability; MiRNA

Indexed keywords

FLUOROURACIL; MICRORNA; MICRORNA 10B; MICRORNA 133B; MICRORNA 23A; MICRORNA 27A; MICRORNA 30C; MICRORNA 31; MICRORNA 486; MICRORNA 625; MICRORNA 99A; UNCLASSIFIED DRUG; ABC TRANSPORTER; ABCF1 PROTEIN, HUMAN; MIRN23 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ABCF1 GENE; ARTICLE; CELL VIABILITY; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROARRAY ANALYSIS; MICROSATELLITE INSTABILITY; PROTEIN BINDING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; APOPTOSIS; CELL SURVIVAL; COLORECTAL TUMOR; DEFICIENCY; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; TUMOR CELL LINE;

APOPTOSIS; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; CELL LINE, TUMOR; CELL SURVIVAL; COLORECTAL NEOPLASMS; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HUMANS; MICRORNAS; MICROSATELLITE INSTABILITY;

EID: 84929621152     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920371604150429153309     Document Type: Article

References (52)

1. [1] Martin, L.P.; Hamilton, T.C.; Schilder, R.J. Platinum resistance: the role of DNA repair pathways. Clin. Cancer Res., 2008, 14(5), 1291-1295.
2. [2] Kunkel, T.A.; Erie, D.A. DNA mismatch repair. Ann. Rev. Biochem., 2005, 74, 681-710.
3. [3] Jascur, T.; Boland, C.R. Structure and function of the components of the human DNA mismatch repair system. Int. J. Cancer., 2006, 119(9), 2030-2035.
4. [4] Martin, S.A.; Lord, C.J.; Ashworth, A. Therapeutic targeting of the DNA mismatch repair pathway. Clin. Cancer Res., 2010, 16(21), 5107-5113.
5. [5] Vilar, E.; Gruber, S.B. Microsatellite instability in colorectal cancer-the stable evidence. Nat. Rev. Clin. Oncol., 2010, 7(3), 153-162.
6. [6] Sargent, D.J.; Marsoni, S.; Monges, G.; Thibodeau, S.N.; Labianca, R.; Hamilton, S.R.; French, A.J.; Kabat, B.; Foster, N.R.; Torri, V.; Ribic, C.; Grothey, A.; Moore, M.; Zaniboni, A.; Seitz, J.F.; Sinicrope, F.; Gallinger, S. Defective mismatch repair as a predictive marker for lack of efficacy of fluorouracil-based adjuvant therapy in colon cancer. J. Clin. Oncol., 2010, 28(20), 3219-3226.
7. [7] Jover, R.; Zapater, P.; Castells, A.; Llor, X.; Andreu, M.; Cubiella, J.; Pinol, V.; Xicola, R.M.; Bujanda, L.; Rene, J.M.; Clofent, J.; Bessa, X.; Morillas, J.D.; Nicolas-Perez, D.; Paya, A.; Alenda, C. Gastrointestinal Oncology Group of the Spanish Gastroenterological, A., Mismatch repair status in the prediction of benefit from adjuvant fluorouracil chemotherapy in colorectal cancer. Gut, 2006, 55(6), 848-855.
8. [8] Pocard, M.; Bras-Goncalves, R.; Hamelin, R.; Northover, J.; Poupon, M.F. Response to 5-fluorouracil of orthotopically xenografted human colon cancers with a microsatellite instability: influence of P53 status. Anticancer Res., 2000, 20(1A), 85-90.
9. [9] Lee, Y.S.; Dutta, A. MicroRNAs in cancer. Annu. Rev. Pathol., 2009, 4, 199-227.
10. [10] Zhang, X.; Chen, J.; Radcliffe, T.; Lebrun, D.P.; Tron, V.A.; Feilotter, H. An array-based analysis of microRNA expression comparing matched frozen and formalin-fixed paraffin-embedded human tissue samples. J. Mol. Diagn., 2008, 10(6), 513-519.
11. [11] Cummins, J.M.; He, Y.; Leary, R.J.; Pagliarini, R.; Diaz, L.A., Jr.; Sjoblom, T.; Barad, O.; Bentwich, Z.; Szafranska, A.E.; Labourier, E.; Raymond, C.K.; Roberts, B.S.; Juhl, H.; Kinzler, K.W.; Vogelstein, B.; Velculescu, V.E. The colorectal microRNAome. Proc. Natl. Acad. Sci. U. S. A., 2006, 103(10), 3687-3692.
12. [12] Earle, J.S.; Luthra, R.; Romans, A.; Abraham, R.; Ensor, J.; Yao, H.; Hamilton, S.R. Association of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. J. Mol. Diagn., 2010, 12(4), 433-440.
13. [13] Lanza, G.; Ferracin, M.; Gafa, R.; Veronese, A.; Spizzo, R.; Pichiorri, F.; Liu, C.G.; Calin, G.A.; Croce, C.M.; Negrini, M. mRNA/microRNA gene expression profile in microsatellite unstable colorectal cancer. Mol. Cancer, 2007, 6, 54.
14. [14] Sarver, A.L.; French, A.J.; Borralho, P.M.; Thayanithy, V.; Oberg, A.L.; Silverstein, K.A.; Morlan, B.W.; Riska, S.M.; Boardman, L.A.; Cunningham, J.M.; Subramanian, S.; Wang, L.; Smyrk, T.C.; Rodrigues, C.M.; Thibodeau, S.N.; Steer, C.J. Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer, 2009, 9, 401.
15. [15] Qu, J.; Zhao, L.; Zhang, P.; Wang, J.; Xu, N.; Mi, W.; Jiang, X.; Zhang, C.; Qu, J. MicroRNA-195 chemosensitizes colon cancer cells to the chemotherapeutic drug doxorubicin by targeting the first binding site of BCL2L2 mRNA. J. Cell Physiol., 2015, 230(3), 535-545.
16. [16] Borralho, P.M.; Kren, B.T.; Castro, R.E.; da Silva, I.B.; Steer, C.J.; Rodrigues, C.M. MicroRNA-143 reduces viability and increases sensitivity to 5-fluorouracil in HCT116 human colorectal cancer cells. FEBS J., 2009, 276(22), 6689-6700.
17. [17] Valeri, N.; Gasparini, P.; Braconi, C.; Paone, A.; Lovat, F.; Fabbri, M.; Sumani, K.M.; Alder, H.; Amadori, D.; Patel, T.; Nuovo, G.J.; Fishel, R.; Croce, C.M. MicroRNA-21 induces resistance to 5-fluorouracil by down-regulating human DNA MutS homolog 2 (hMSH2). Proc. Natl. Acad. Sci. U. S. A., 2010, 107(49), 21098-21103.
18. [18] Zhong, Z.; Dong, Z.; Yang, L.; Chen, X.; Gong, Z. MicroRNA-31-5p modulates cell cycle by targeting human mutL homolog 1 in human cancer cells. Tumour Biol., 2013, 34(3), 1959-1965.
19. [19] Wang, L.L.; Liu, Y.H.; Meng, L.L.; Li, C.G.; Zhou, S.F. Phenotype prediction of non-synonymous single-nucleotide polymorphisms in human ATP-binding cassette transporter genes. Basic Clin. Pharmacol. Toxicol., 2011, 108(2), 94-114.
20. [20] Cole, S.P.; Bhardwaj, G.; Gerlach, J.H.; Mackie, J.E.; Grant, C.E.; Almquist, K.C.; Stewart, A.J.; Kurz, E.U.; Duncan, A.M.; Deeley, R.G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science, 1992, 258(5088), 1650-1654.
21. [21] Paladini, F.; Belfiore, F.; Cocco, E.; Carcassi, C.; Cauli, A.; Vacca, A.; Fiorillo, M.T.; Mathieu, A.; Cascino, I.; Sorrentino, R. HLA-E gene polymorphism associates with ankylosing spondylitis in Sardinia. Arthritis Res. Ther., 2009, 11(6), R171.
22. [22] Richard, M.; Drouin, R.; Beaulieu, A.D. ABC50, a novel human ATP-binding cassette protein found in tumor necrosis factor-alphastimulated synoviocytes. Genomics, 1998, 53(2), 137-145.
23. [23] Hlavata, I.; Mohelnikova-Duchonova, B.; Vaclavikova, R.; Liska, V.; Pitule, P.; Novak, P.; Bruha, J.; Vycital, O.; Holubec, L.; Treska, V.; Vodicka, P.; Soucek, P. The role of ABC transporters in progression and clinical outcome of colorectal cancer. Mutagenesis, 2012, 27(2), 187-196.
24. [24] Mei, Q.; Li, X.; Meng, Y.; Wu, Z.; Guo, M.; Zhao, Y.; Fu, X.; Han, W. A facile and specific assay for quantifying microRNA by an optimized RT-qPCR approach. PloS one, 2012, 7(10), e46890.
25. [25] Shang, J.; Yang, F.; Wang, Y.; Wang, Y.; Xue, G.; Mei, Q.; Wang, F.; Sun, S. MicroRNA-23a antisense enhances 5-fluorouracil chemosensitivity through APAF-1/caspase-9 apoptotic pathway in colorectal cancer cells. J. Cell Biochem., 2014, 115(4), 772-784.
26. [26] O'Donnell, K.A.; Wentzel, E.A.; Zeller, K.I.; Dang, C.V.; Mendell, J.T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature, 2005, 435(7043), 839-843.
27. [27] Johnson, S.M.; Grosshans, H.; Shingara, J.; Byrom, M.; Jarvis, R.; Cheng, A.; Labourier, E.; Reinert, K.L.; Brown, D.; Slack, F.J. RAS is regulated by the let-7 microRNA family. Cell, 2005, 120(5), 635-647.
28. [28] To, K.K.; Zhan, Z.; Litman, T.; Bates, S.E. 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, 2008, 28(17), 5147-5161.
29. [29] Pan, Y.Z.; Morris, M.E.; Yu, A.M. MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells. Mol. Pharmacol., 2009, 75(6), 1374-1379.
30. [30] Zhu, H.; Wu, H.; Liu, X.; Evans, B.R.; Medina, D.J.; Liu, C.G.; Yang, J.M. Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem. Pharmacol., 2008, 76(5), 582-588.
31. [31] Kinzler, K.W.; Vogelstein, B. Lessons from hereditary colorectal cancer. Cell, 1996, 87(2), 159-170.
32. [32] Duval, A.; Hamelin, R. Mutations at coding repeat sequences in mismatch repair-deficient human cancers: toward a new concept of target genes for instability. Cancer Res., 2002, 62(9), 2447-2454.
33. [33] Hampel, H.; Frankel, W.L.; Martin, E.; Arnold, M.; Khanduja, K.; Kuebler, P.; Nakagawa, H.; Sotamaa, K.; Prior, T.W.; Westman, J.; Panescu, J.; Fix, D.; Lockman, J.; Comeras, I.; de la Chapelle, A. Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer). N. Engl. J. Med., 2005, 352(18), 1851-1860.
34. [34] Truninger, K.; Menigatti, M.; Luz, J.; Russell, A.; Haider, R.; Gebbers, J.O.; Bannwart, F.; Yurtsever, H.; Neuweiler, J.; Riehle, H.M.; Cattaruzza, M.S.; Heinimann, K.; Schar, P.; Jiricny, J.; Marra, G. Immunohistochemical analysis reveals high frequency of PMS2 defects in colorectal cancer. Gastroenterology, 2005, 128(5), 1160-1171.
35. [35] Jass, J.R.; Do, K.A.; Simms, L.A.; Iino, H.; Wynter, C.; Pillay, S.P.; Searle, J.; Radford-Smith, G.; Young, J.; Leggett, B. Morphology of sporadic colorectal cancer with DNA replication errors. Gut, 1998, 42(5), 673-679.
36. [36] Gryfe, R.; Kim, H.; Hsieh, E.T.; Aronson, M.D.; Holowaty, E.J.; Bull, S.B.; Redston, M.; Gallinger, S. Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N. Engl. J. Med., 2000, 342, (2), 69-77.
37. [37] Popat, S.; Hubner, R.; Houlston, R.S. Systematic review of microsatellite instability and colorectal cancer prognosis. J. Clin. Oncol., 2005, 23(3), 609-618.
38. [38] Ribic, C.M.; Sargent, D.J.; Moore, M.J.; Thibodeau, S.N.; French, A.J.; Goldberg, R.M.; Hamilton, S.R.; Laurent-Puig, P.; Gryfe, R.; Shepherd, L.E.; Tu, D.; Redston, M.; Gallinger, S. Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer. N. Engl. J. Med., 2003, 349(3), 247-257.
39. [39] Carethers, J.M.; Chauhan, D.P.; Fink, D.; Nebel, S.; Bresalier, R.S.; Howell, S.B.; Boland, C.R. Mismatch repair proficiency and in vitro response to 5-fluorouracil. Gastroenterology, 1999, 117(1), 123-131.
40. [40] Lujambio, A.; Lowe, S.W. The microcosmos of cancer. Nature, 2012, 482(7385), 347-355.
41. [41] Valeri, N.; Gasparini, P.; Fabbri, M.; Braconi, C.; Veronese, A.; Lovat, F.; Adair, B.; Vannini, I.; Fanini, F.; Bottoni, A.; Costinean, S.; Sandhu, S.K.; Nuovo, G.J.; Alder, H.; Gafa, R.; Calore, F.; Ferracin, M.; Lanza, G.; Volinia, S.; Negrini, M.; McIlhatton, M.A.; Amadori, D.; Fishel, R.; Croce, C.M. Modulation of mismatch repair and genomic stability by miR-155. Proc. Natl. Acad. Sci. U. S. A., 2010, 107(15), 6982-6987.
42. [42] Ng, E.K.; Chong, W.W.; Jin, H.; Lam, E.K.; Shin, V.Y.; Yu, J.; Poon, T.C.; Ng, S.S.; Sung, J.J. Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut, 2009, 58(10), 1375-1381.
43. [43] Volinia, S.; Calin, G.A.; Liu, C.G.; Ambs, S.; Cimmino, A.; Petrocca, F.; Visone, R.; Iorio, M.; Roldo, C.; Ferracin, M.; Prueitt, R.L.; Yanaihara, N.; Lanza, G.; Scarpa, A.; Vecchione, A.; Negrini, M.; Harris, C.C.; Croce, C.M. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. U. S. A., 2006, 103(7), 2257-2261.
44. [44] Luo, X.; Burwinkel, B.; Tao, S.; Brenner, H. MicroRNA signatures: novel biomarker for colorectal cancer? Cancer Epidemiol. Biomarkers Prev., 2011, 20(7), 1272-1286.
45. [45] Wickramasinghe, N.S.; Manavalan, T.T.; Dougherty, S.M.; Riggs, K.A.; Li, Y.; Klinge, C.M. Estradiol downregulates miR-21 expression and increases miR-21 target gene expression in MCF-7 breast cancer cells. Nucleic Acids Res., 2009, 37(8), 2584-2595.
46. [46] Asangani, I.A.; Rasheed, S.A.; Nikolova, D.A.; Leupold, J.H.; Colburn, N.H.; Post, S.; Allgayer, H. MicroRNA-21 (miR-21) posttranscriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene, 2008, 27(15), 2128-2136.
47. [47] Meng, F.; Henson, R.; Lang, M.; Wehbe, H.; Maheshwari, S.; Mendell, J.T.; Jiang, J.; Schmittgen, T.D.; Patel, T. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology, 2006, 130(7), 2113-2129.
48. [48] Allen, K.E.; Weiss, G.J. Resistance may not be futile: microRNA biomarkers for chemoresistance and potential therapeutics. Mol. Cancer Ther., 2010, 9(12), 3126-3136.
49. [49] Blower, P.E.; Chung, J.H.; Verducci, J.S.; Lin, S.; Park, J.K.; Dai, Z.; Liu, C.G.; Schmittgen, T.D.; Reinhold, W.C.; Croce, C.M.; Weinstein, J.N.; Sadee, W. MicroRNAs modulate the chemosensitivity of tumor cells. Mol. Cancer Ther., 2008, 7(1), 1-9.
50. [50] Chhabra, R.; Dubey, R.; Saini, N. Cooperative and individualistic functions of the microRNAs in the miR-23a~27a~24-2 cluster and its implication in human diseases. Mol. Cancer, 2010, 9, 232.
51. [51] Yu, H.W.; Sze, D.M.; Cho, W.C. MicroRNAs Involved in Anti-Tumour Immunity. Int. J. Mol. Sci., 2013, 14(3), 5587-5607.
52. [52] Taki, K.; Fukushima, T.; Ise, R.; Horii, I.; Yoshida, T. Microarray analysis of 6-mercaptopurine-induced-toxicity-related genes and microRNAs in the rat placenta. J. Toxicol. Sci., 2013, 38(1), 159-167.