Advertisement

Tumor Biology

, Volume 37, Issue 10, pp 12905–12913 | Cite as

MiRNAs-mediated cisplatin resistance in breast cancer

  • Xiu Chen
  • Peng Lu
  • Ying Wu
  • Dan-dan Wang
  • Siying Zhou
  • Su-jin Yang
  • Hong-Yu Shen
  • Xiao-hui Zhang
  • Jian-hua Zhao
  • Jin-hai Tang
Review

Abstract

Cisplatin is a widely used chemotherapeutic agent in breast cancer treatments with inevitable rapidly acquired resistance or intrinsically resistance. Enormous evidence points to the bioprocesses of resistant formation consisting of diverse miRNAs direct and indirect actions on relevant encoding genes. In this report, we overview detailed information on the miRNAs effect on cisplatin-induced resistance, including alterations in cell survival, modification of DNA damage response, changes in cellular uptake or efflux of the drug, altered DNA methylation, and perturbations in the miRNA biogenesis pathway. This will provide potential miRNA-targeted strategies for the treatment of breast cancer therapy and requires further clinical application.

Keywords

miRNAs Cisplatin Drug resistance Breast 

Notes

Acknowledgments

This study was funded by the National Natural Science Foundation of China (grant number 81272470). We thank Shan-liang Zhong for his help in revision of the present paper.

Compliance with ethical standards

Conflicts of interest

None

References

  1. 1.
    Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86. doi: 10.1002/ijc.29210.CrossRefPubMedGoogle Scholar
  2. 2.
    DeSantis CE, Fedewa SA, Goding Sauer A, Kramer JL, Smith RA, Jemal A. Breast cancer statistics, 2015: convergence of incidence rates between black and white women. CA Cancer J Clin. 2015. doi: 10.3322/caac.21320.Google Scholar
  3. 3.
    Perou CM. Molecular stratification of triple-negative breast cancers. Oncologist. 2011;16(Suppl 1):61–70. doi: 10.1634/theoncologist.2011-S1-61.CrossRefPubMedGoogle Scholar
  4. 4.
    Prat A, Perou CM. Deconstructing the molecular portraits of breast cancer. Mol Oncol. 2011;5(1):5–23. doi: 10.1016/j.molonc.2010.11.003.CrossRefPubMedGoogle Scholar
  5. 5.
    Harrell JC, Prat A, Parker JS, Fan C, He X, Carey L, et al. Genomic analysis identifies unique signatures predictive of brain, lung, and liver relapse. Breast Cancer Res Treat. 2012;132(2):523–35. doi: 10.1007/s10549-011-1619-7.CrossRefPubMedGoogle Scholar
  6. 6.
    Poklar N, Pilch DS, Lippard SJ, Redding EA, Dunham SU, Breslauer KJ. Influence of cisplatin intrastrand crosslinking on the conformation, thermal stability, and energetics of a 20-mer DNA duplex. Proc Natl Acad Sci U S A. 1996;93(15):7606–11.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Rudd GN, Hartley JA, Souhami RL. Persistence of cisplatin-induced DNA interstrand crosslinking in peripheral blood mononuclear cells from elderly and young individuals. Cancer Chemother Pharmacol. 1995;35(4):323–6. doi: 10.1007/bf00689452.CrossRefPubMedGoogle Scholar
  8. 8.
    O’Driscoll L, Clynes M. Biomarkers and multiple drug resistance in breast cancer. Curr Cancer Drug Targets. 2006;6(5):365–84.CrossRefPubMedGoogle Scholar
  9. 9.
    Ma J, Dong C, Ji C. MicroRNA and drug resistance. Cancer Gene Ther. 2010;17(8):523–31. doi: 10.1038/cgt.2010.18.CrossRefPubMedGoogle Scholar
  10. 10.
    Kutanzi KR, Yurchenko OV, Beland FA, Checkhun VF, Pogribny IP. MicroRNA-mediated drug resistance in breast cancer. Clin Epigenet. 2011;2(2):171–85. doi: 10.1007/s13148-011-0040-8.CrossRefGoogle Scholar
  11. 11.
    Yokoi T, Nakajima M. microRNAs as mediators of drug toxicity. Annu Rev Pharmacol Toxicol. 2013;53:377–400. doi: 10.1146/annurev-pharmtox-011112-140250.CrossRefPubMedGoogle Scholar
  12. 12.
    Yu DD, Lv MM, Chen WX, Zhong SL, Zhang XH, Chen L, et al. Role of miR-155 in drug resistance of breast cancer. Tumour Biol. 2015;36(3):1395–401. doi: 10.1007/s13277-015-3263-z.CrossRefPubMedGoogle Scholar
  13. 13.
    Koberle B, Tomicic MT, Usanova S, Kaina B. Cisplatin resistance: preclinical findings and clinical implications. Biochim Biophys Acta. 2010;1806(2):172–82. doi: 10.1016/j.bbcan.2010.07.004.PubMedGoogle Scholar
  14. 14.
    Shen DW, Pouliot LM, Hall MD, Gottesman MM. Cisplatin resistance: a cellular self-defense mechanism resulting from multiple epigenetic and genetic changes. Pharmacol Rev. 2012;64(3):706–21. doi: 10.1124/pr.111.005637.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Peng B, Gu Y, Xiong Y, Zheng G, He Z. Microarray-assisted pathway analysis identifies MT1X & NFkappaB as mediators of TCRP1-associated resistance to cisplatin in oral squamous cell carcinoma. PLoS One. 2012;7(12):e51413. doi: 10.1371/journal.pone.0051413.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):11–30. doi: 10.3322/caac.21166.CrossRefPubMedGoogle Scholar
  17. 17.
    Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, et al. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31(15):1869–83. doi: 10.1038/onc.2011.384.CrossRefPubMedGoogle Scholar
  18. 18.
    Fuertes MA, Castilla J, Alonso C, Perez JM. Cisplatin biochemical mechanism of action: from cytotoxicity to induction of cell death through interconnections between apoptotic and necrotic pathways. Curr Med Chem. 2003;10(3):257–66.CrossRefPubMedGoogle Scholar
  19. 19.
    Liu FS. Mechanisms of chemotherapeutic drug resistance in cancer therapy—a quick review. Taiwan J Obstet Gynecol. 2009;48(3):239–44. doi: 10.1016/S1028-4559(09)60296-5.CrossRefPubMedGoogle Scholar
  20. 20.
    Peng B, Yi S, Gu Y, Zheng G, He Z. Purification and biochemical characterization of a novel protein-tongue cancer chemotherapy resistance-associated protein1 (TCRP1). Protein Expr Purif. 2012;82(2):360–7. doi: 10.1016/j.pep.2012.02.002.CrossRefPubMedGoogle Scholar
  21. 21.
    Pogribny IP, Filkowski JN, Tryndyak VP, Golubov A, Shpyleva SI, Kovalchuk O. Alterations of microRNAs and their targets are associated with acquired resistance of MCF-7 breast cancer cells to cisplatin. Int J Cancer. 2010;127(8):1785–94. doi: 10.1002/ijc.25191.CrossRefPubMedGoogle Scholar
  22. 22.
    Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, et al. RAS is regulated by the let-7 microRNA family. Cell. 2005;120(5):635–47. doi: 10.1016/j.cell.2005.01.014.CrossRefPubMedGoogle Scholar
  23. 23.
    Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 2004;64(11):3753–6. doi: 10.1158/0008-5472.can-04-0637.CrossRefPubMedGoogle Scholar
  24. 24.
    Yang N, Kaur S, Volinia S, Greshock J, Lassus H, Hasegawa K, et al. MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res. 2008;68(24):10307–14. doi: 10.1158/0008-5472.can-08-1954.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Kumar MS, Erkeland SJ, Pester RE, Chen CY, Ebert MS, Sharp PA, et al. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci U S A. 2008;105(10):3903–8. doi: 10.1073/pnas.0712321105.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 2007;131(6):1109–23. doi: 10.1016/j.cell.2007.10.054.CrossRefPubMedGoogle Scholar
  27. 27.
    Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 2007;21(9):1025–30. doi: 10.1101/gad.1540407.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Peng Y, Laser J, Shi G, Mittal K, Melamed J, Lee P, et al. Antiproliferative effects by Let-7 repression of high-mobility group A2 in uterine leiomyoma. Mol Cancer Res: MCR. 2008;6(4):663–73. doi: 10.1158/1541-7786.MCR-07-0370.CrossRefPubMedGoogle Scholar
  29. 29.
    Mayr C, Hemann MT, Bartel DP. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science. 2007;315(5818):1576–9. doi: 10.1126/science.1137999.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D, et al. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res. 2007;67(16):7713–22. doi: 10.1158/0008-5472.can-07-1083.CrossRefPubMedGoogle Scholar
  31. 31.
    Schultz J, Lorenz P, Gross G, Ibrahim S, Kunz M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res. 2008;18(5):549–57. doi: 10.1038/cr.2008.45.CrossRefPubMedGoogle Scholar
  32. 32.
    Yang L, Zhou Y, Li Y, Zhou J, Wu Y, Cui Y, et al. Mutations of p53 and KRAS activate NF-kappaB to promote chemoresistance and tumorigenesis via dysregulation of cell cycle and suppression of apoptosis in lung cancer cells. Cancer Lett. 2015;357(2):520–6. doi: 10.1016/j.canlet.2014.12.003.CrossRefPubMedGoogle Scholar
  33. 33.
    Tao S, Wang S, Moghaddam SJ, Ooi A, Chapman E, Wong PK, et al. Oncogenic KRAS confers chemoresistance by upregulating NRF2. Cancer Res. 2014;74(24):7430–41. doi: 10.1158/0008-5472.can-14-1439.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Yan X, Shen H, Jiang H, Hu D, Wang J, Wu X. External Qi of Yan Xin Qigong inhibits activation of Akt, Erk1/2 and NF-kB and induces cell cycle arrest and apoptosis in colorectal cancer cells. Cell Physiol Biochem. 2013;31(1):113–22. doi: 10.1159/000343354.CrossRefPubMedGoogle Scholar
  35. 35.
    Shin SM, Yang JH, Ki SH. Role of the Nrf2-ARE pathway in liver diseases. Oxidative Med Cell Longev. 2013;2013:763257. doi: 10.1155/2013/763257.CrossRefGoogle Scholar
  36. 36.
    Reddy NM, Kleeberger SR, Bream JH, Fallon PG, Kensler TW, Yamamoto M, et al. Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling. Oncogene. 2008;27(44):5821–32. doi: 10.1038/onc.2008.188.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kim SK, Yang JW, Kim MR, Roh SH, Kim HG, Lee KY, et al. Increased expression of Nrf2/ARE-dependent anti-oxidant proteins in tamoxifen-resistant breast cancer cells. Free Radic Biol Med. 2008;45(4):537–46. doi: 10.1016/j.freeradbiomed.2008.05.011.CrossRefPubMedGoogle Scholar
  38. 38.
    Kumar S, Kumar A, PP S, SN R, SK P, SS K. MicroRNA signature of cis-platin resistant vs. cis-platin sensitive ovarian cancer cell lines. J Ovarian Res. 2011;4(1):17. doi: 10.1186/1757-2215-4-17.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Boo LM, Lin HH, Chung V, Zhou B, Louie SG, O’Reilly MA, et al. High mobility group A2 potentiates genotoxic stress in part through the modulation of basal and DNA damage-dependent phosphatidylinositol 3-kinase-related protein kinase activation. Cancer Res. 2005;65(15):6622–30. doi: 10.1158/0008-5472.can-05-0086.CrossRefPubMedGoogle Scholar
  40. 40.
    Louis M, Rosato RR, Brault L, Osbild S, Battaglia E, Yang XH, et al. The histone deacetylase inhibitor sodium butyrate induces breast cancer cell apoptosis through diverse cytotoxic actions including glutathione depletion and oxidative stress. Int J Oncol. 2004;25(6):1701–11.PubMedGoogle Scholar
  41. 41.
    Saha P, Eichbaum Q, Silberman ED, Mayer BJ, Dutta A. p21CIP1 and Cdc25A: competition between an inhibitor and an activator of cyclin-dependent kinases. Mol Cell Biol. 1997;17(8):4338–45.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Hoffmann I, Draetta G, Karsenti E. Activation of the phosphatase activity of human cdc25A by a cdk2-cyclin E dependent phosphorylation at the G1/S transition. EMBO J. 1994;13(18):4302–10.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Jinno S, Suto K, Nagata A, Igarashi M, Kanaoka Y, Nojima H, et al. Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J. 1994;13(7):1549–56.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Cangi MG, Cukor B, Soung P, Signoretti S, Moreira Jr G, Ranashinge M, et al. Role of the Cdc25A phosphatase in human breast cancer. J Clin Invest. 2000;106(6):753–61. doi: 10.1172/jci9174.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science. 2007;318(5858):1931–4. doi: 10.1126/science.1149460.CrossRefPubMedGoogle Scholar
  46. 46.
    Hernandez-Vargas H, Rodriguez-Pinilla SM, Julian-Tendero M, Sanchez-Rovira P, Cuevas C, Anton A, et al. Gene expression profiling of breast cancer cells in response to gemcitabine: NF-kappaB pathway activation as a potential mechanism of resistance. Breast Cancer Res Treat. 2007;102(2):157–72. doi: 10.1007/s10549-006-9322-9.CrossRefPubMedGoogle Scholar
  47. 47.
    Chaluvally-Raghavan P, Zhang F, Pradeep S, Hamilton Mark P, Zhao X, Rupaimoole R, et al. Copy number gain of hsa-miR-569 at 3q26.2 leads to loss of TP53INP1 and aggressiveness of epithelial cancers. Cancer Cell. 2014;26(6):863–79. doi: 10.1016/j.ccell.2014.10.010.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Liang Y, McDonnell S, Clynes M. Examining the relationship between cancer invasion/metastasis and drug resistance. Curr Cancer Drug Targets. 2002;2(3):257–77.CrossRefPubMedGoogle Scholar
  49. 49.
    Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10(5):593–601. doi: 10.1038/ncb1722.CrossRefPubMedGoogle Scholar
  50. 50.
    Paterson EL, Kolesnikoff N, Gregory PA, Bert AG, Khew-Goodall Y, Goodall GJ. The microRNA-200 family regulates epithelial to mesenchymal transition. TheScientificWorldJOURNAL. 2008;8:901–4. doi: 10.1100/tsw.2008.115.CrossRefPubMedGoogle Scholar
  51. 51.
    Agiostratidou G, Hulit J, Phillips GR, Hazan RB. Differential cadherin expression: potential markers for epithelial to mesenchymal transformation during tumor progression. J Mammary Gland Biol Neoplasia. 2007;12(2–3):127–33. doi: 10.1007/s10911-007-9044-6.CrossRefPubMedGoogle Scholar
  52. 52.
    Schwarzenbach H, Milde-Langosch K, Steinbach B, Muller V, Pantel K. Diagnostic potential of PTEN-targeting miR-214 in the blood of breast cancer patients. Breast Cancer Res Treat. 2012;134(3):933–41. doi: 10.1007/s10549-012-1988-6.CrossRefPubMedGoogle Scholar
  53. 53.
    Yang H, Kong W, He L, Zhao JJ, O’Donnell JD, Wang J, et al. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 2008;68(2):425–33. doi: 10.1158/0008-5472.can-07-2488.CrossRefPubMedGoogle Scholar
  54. 54.
    van Jaarsveld MT, Wouters MD, Boersma AW, Smid M, van Ijcken WF, Mathijssen RH, et al. DNA damage responsive microRNAs misexpressed in human cancer modulate therapy sensitivity. Mol Oncol. 2014;8(3):458–68. doi: 10.1016/j.molonc.2013.12.011.CrossRefPubMedGoogle Scholar
  55. 55.
    Hoeijmakers JH. DNA damage, aging, and cancer. N Engl J Med. 2009;361(15):1475–85. doi: 10.1056/NEJMra0804615.CrossRefPubMedGoogle Scholar
  56. 56.
    Rodier F, Munoz DP, Teachenor R, Chu V, Le O, Bhaumik D, et al. DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. J Cell Sci. 2011;124(Pt 1):68–81. doi: 10.1242/jcs.071340.CrossRefPubMedGoogle Scholar
  57. 57.
    Port M, Glaesener S, Ruf C, Riecke A, Bokemeyer C, Meineke V, et al. Micro-RNA expression in cisplatin resistant germ cell tumor cell lines. Mol Cancer. 2011;10:52. doi: 10.1186/1476-4598-10-52.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Sangster-Guity N, Conrad BH, Papadopoulos N, Bunz F. ATR mediates cisplatin resistance in a p53 genotype-specific manner. Oncogene. 2011;30(22):2526–33. doi: 10.1038/onc.2010.624.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Ru P, Steele R, Hsueh EC, Ray RB. Anti-miR-203 upregulates SOCS3 expression in breast cancer cells and enhances cisplatin chemosensitivity. Genes Cancer. 2011;2(7):720–7. doi: 10.1177/1947601911425832.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Qin LF, Ng IO. Exogenous expression of p21(WAF1/CIP1) exerts cell growth inhibition and enhances sensitivity to cisplatin in hepatoma cells. Cancer Lett. 2001;172(1):7–15.CrossRefPubMedGoogle Scholar
  61. 61.
    O’Brien K, Lowry MC, Corcoran C, Martinez VG, Daly M, Rani S et al. miR-134 in extracellular vesicles reduces triple-negative breast cancer aggression and increases drug sensitivity. Oncotarget. 2015.Google Scholar
  62. 62.
    Perotti C, Liu R, Parusel CT, Bocher N, Schultz J, Bork P, et al. Heat shock protein-90-alpha, a prolactin-STAT5 target gene identified in breast cancer cells, is involved in apoptosis regulation. Breast Cancer Res. 2008;10(6):R94. doi: 10.1186/bcr2193.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Workman P, Burrows F, Neckers L, Rosen N. Drugging the cancer chaperone HSP90: combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann N Y Acad Sci. 2007;1113:202–16. doi: 10.1196/annals.1391.012.CrossRefPubMedGoogle Scholar
  64. 64.
    Gallerne C, Prola A, Lemaire C. Hsp90 inhibition by PU-H71 induces apoptosis through endoplasmic reticulum stress and mitochondrial pathway in cancer cells and overcomes the resistance conferred by Bcl-2. Biochim Biophys Acta. 2013;1833(6):1356–66. doi: 10.1016/j.bbamcr.2013.02.014.CrossRefPubMedGoogle Scholar
  65. 65.
    Jiang Q, Greenberg RA. Deciphering the BRCA1 tumor suppressor network. J Biol Chem. 2015;290(29):17724–32. doi: 10.1074/jbc.R115.667931.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    He X, Xiao X, Dong L, Wan N, Zhou Z, Deng H, et al. MiR-218 regulates cisplatin chemosensitivity in breast cancer by targeting BRCA1. Tumour Biol. 2015;36(3):2065–75. doi: 10.1007/s13277-014-2814-z.CrossRefPubMedGoogle Scholar
  67. 67.
    Tan X, Peng J, Fu Y, An S, Rezaei K, Tabbara S, et al. miR-638 mediated regulation of BRCA1 affects DNA repair and sensitivity to UV and cisplatin in triple-negative breast cancer. Breast Cancer Res. 2014;16(5):435. doi: 10.1186/s13058-014-0435-5.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Stordal B, Davey R. A systematic review of genes involved in the inverse resistance relationship between cisplatin and paclitaxel chemotherapy: role of BRCA1. Curr Cancer Drug Targets. 2009;9(3):354–65.CrossRefPubMedGoogle Scholar
  69. 69.
    Pauwels EK, Erba P, Mariani G, Gomes CM. Multidrug resistance in cancer: its mechanism and its modulation. Drug News Perspect. 2007;20(6):371–7. doi: 10.1358/dnp.2007.20.6.1141496.CrossRefPubMedGoogle Scholar
  70. 70.
    Borst P, Evers R, Kool M, Wijnholds J. A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst. 2000;92(16):1295–302.CrossRefPubMedGoogle Scholar
  71. 71.
    Siddik ZH. Biochemical and molecular mechanisms of cisplatin resistance. Cancer Treat Res. 2002;112:263–84.CrossRefPubMedGoogle Scholar
  72. 72.
    Siddik ZH. Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene. 2003;22(47):7265–79. doi: 10.1038/sj.onc.1206933.CrossRefPubMedGoogle Scholar
  73. 73.
    Negoro K, Yamano Y, Fushimi K, Saito K, Nakatani K, Shiiba M, et al. Establishment and characterization of a cisplatin-resistant cell line, KB-R, derived from oral carcinoma cell line, KB. Int J Oncol. 2007;30(6):1325–32.PubMedGoogle Scholar
  74. 74.
    Louisa M, Soediro TM, Suyatna FD. In vitro modulation of P-glycoprotein, MRP-1 and BCRP expression by mangiferin in doxorubicin-treated MCF-7 cells. Asian Pacific J Cancer Prev: APJCP. 2014;15(4):1639–42.CrossRefGoogle Scholar
  75. 75.
    Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A. 2007;104(40):15805–10. doi: 10.1073/pnas.0707628104.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Su Y, Wang X, Li J, Xu J, Xu L. The clinicopathological significance and drug target potential of FHIT in breast cancer, a meta-analysis and literature review. Drug Des Dev Ther. 2015;9:5439–45. doi: 10.2147/dddt.s89861.Google Scholar
  77. 77.
    Li J, Liu J, Ren Y, Liu P. Roles of the WWOX in pathogenesis and endocrine therapy of breast cancer. Exp Biol Med (Maywood, NJ). 2015;240(3):324–8. doi: 10.1177/1535370214561587.CrossRefGoogle Scholar
  78. 78.
    Koturbash I, Boyko A, Rodriguez-Juarez R, McDonald RJ, Tryndyak VP, Kovalchuk I, et al. Role of epigenetic effectors in maintenance of the long-term persistent bystander effect in spleen in vivo. Carcinogenesis. 2007;28(8):1831–8. doi: 10.1093/carcin/bgm053.CrossRefPubMedGoogle Scholar
  79. 79.
    Klein ME, Lioy DT, Ma L, Impey S, Mandel G, Goodman RH. Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat Neurosci. 2007;10(12):1513–4. doi: 10.1038/nn2010.CrossRefPubMedGoogle Scholar
  80. 80.
    Kohno K, Wang KY, Takahashi M, Kurita T, Yoshida Y, Hirakawa M, et al. Mitochondrial transcription factor a and mitochondrial genome as molecular targets for cisplatin-based cancer chemotherapy. Int J Mol Sci. 2015;16(8):19836–50. doi: 10.3390/ijms160819836.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Kimura T, Kitada S, Uramoto H, Zhi L, Kawatsu Y, Takeda T, et al. The combination of strong immunohistochemical mtTFA expression and a high survivin index predicts a shorter disease-specific survival in pancreatic ductal adenocarcinoma. Histol Histopathol. 2015;30(2):193–204.PubMedGoogle Scholar
  82. 82.
    Nakayama Y, Yamauchi M, Minagawa N, Torigoe T, Izumi H, Kohno K, et al. Clinical significance of mitochondrial transcription factor A expression in patients with colorectal cancer. Oncol Rep. 2012;27(5):1325–30. doi: 10.3892/or.2012.1640.PubMedGoogle Scholar
  83. 83.
    Yao J, Zhou E, Wang Y, Xu F, Zhang D, Zhong D. microRNA-200a inhibits cell proliferation by targeting mitochondrial transcription factor A in breast cancer. DNA Cell Biol. 2014;33(5):291–300. doi: 10.1089/dna.2013.2132.CrossRefPubMedGoogle Scholar
  84. 84.
    Yao YS, Qiu WS, Yao RY, Zhang Q, Zhuang LK, Zhou F, et al. miR-141 confers docetaxel chemoresistance of breast cancer cells via regulation of EIF4E expression. Oncol Rep. 2015;33(5):2504–12. doi: 10.3892/or.2015.3866.PubMedGoogle Scholar
  85. 85.
    Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature. 2003;425(6956):415–9. doi: 10.1038/nature01957.CrossRefPubMedGoogle Scholar
  86. 86.
    Chan YT, Lin YC, Lin RJ, Kuo HH, Thang WC, Chiu KP, et al. Concordant and discordant regulation of target genes by miR-31 and its isoforms. PLoS One. 2013;8(3):e58169. doi: 10.1371/journal.pone.0058169.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S, et al. A microRNA targeting dicer for metastasis control. Cell. 2010;141(7):1195–207. doi: 10.1016/j.cell.2010.05.017.CrossRefPubMedGoogle Scholar
  88. 88.
    Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 2006;20(16):2202–7. doi: 10.1101/gad.1444406.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2016

Authors and Affiliations

  • Xiu Chen
    • 1
    • 2
  • Peng Lu
    • 3
  • Ying Wu
    • 4
  • Dan-dan Wang
    • 2
  • Siying Zhou
    • 2
  • Su-jin Yang
    • 1
    • 2
  • Hong-Yu Shen
    • 1
    • 2
  • Xiao-hui Zhang
    • 5
  • Jian-hua Zhao
    • 5
  • Jin-hai Tang
    • 2
  1. 1.The Fourth Clinical School of Nanjing Medical UniversityNanjingChina
  2. 2.Department of General SurgeryJiangsu Cancer Hospital Affiliated to Nanjing Medical University and First Affiliated Hospital of Nanjing Medical UniversityNanjingChina
  3. 3.School of Public Health Nanjing Medical UniversityNanjingChina
  4. 4.The First Clinical School of Nanjing Medical UniversityNanjingChina
  5. 5.Center of Clinical Laboratory ScienceJiangsu Cancer Hospital Affiliated to Nanjing Medical UniversityNanjingChina

Personalised recommendations