MiR-20a-5p represses multi-drug resistance in osteosarcoma by targeting the KIF26B gene

Cancer Cell International

Volumn 16, Issue 1, 2016, Pages

  Pu, Youguang ^a   Yi, Qiyi ^a   Zhao, Fangfang ^a   Wang, Haiyan ^b   Cai, Wenjing ^c   Cai, Shanbao ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b ANHUI PROVINCIAL HOSPITAL   (China)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

KIF26B; MiR 20a 5p; Multi drug resistance; Osteosarcoma

Indexed keywords

CARBOPLATIN; CISPLATIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOXORUBICIN; ETOPOSIDE; KINESIN; KINESIN FAMILY MEMBER 26B; METHOTREXATE; MICRORNA 20A; MICRORNA 20A 5P; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; KIF26B GENE; MALE; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; OSTEOSARCOMA; SIGNAL TRANSDUCTION;

EID: 84988412562     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/s12935-016-0340-3     Document Type: Article

References (74)

1. Mirabello L, Troisi RJ, Savage SA. Osteosarcoma incidence and survival rates from 1973 to 2004: data from the surveillance, epidemiology, and end results program. Cancer. 2009;115(7):1531-43.
2. Eilber FR, Rosen G. Adjuvant chemotherapy for osteosarcoma. Semin Oncol. 1989;16(4):312-22.
3. Sakamoto A, Iwamoto Y. Current status and perspectives regarding the treatment of osteo-sarcoma: chemotherapy. Rev Recent Clin Trials. 2008;3(3):228-31.
4. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov. 2006;5(3):219-34.
5. Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell. 2002;108(2):153-64.
6. Rabik CA, Dolan ME. Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev. 2007;33(1):9-23.
7. Sheikh MS, Fornace AJ Jr. Regulation of translation initiation following stress. Oncogene. 1999;18(45):6121-8.
8. Chu E, Copur SM, Ju J, Chen TM, Khleif S, Voeller DM, Mizunuma N, Patel M, Maley GF, Maley F, et al. Thymidylate synthase protein and p53 mRNA form an in vivo ribonucleoprotein complex. Mol Cell Biol. 1999;19(2):1582-94.
9. Ju J, Pedersen-Lane J, Maley F, Chu E. Regulation of p53 expression by thymidylate synthase. Proc Natl Acad Sci USA. 1999;96(7):3769-74.
10. Ju J, Huang C, Minskoff SA, Mayotte JE, Taillon BE, Simons JF. Simultaneous gene expression analysis of steady-state and actively translated mRNA populations from osteosarcoma MG-63 cells in response to IL-1alpha via an open expression analysis platform. Nucleic Acids Res. 2003;31(17):5157-66.
11. Fu L, Minden MD, Benchimol S. Translational regulation of human p53 gene expression. EMBO J. 1996;15(16):4392-401.
12. Chu E, Koeller DM, Casey JL, Drake JC, Chabner BA, Elwood PC, Zinn S, Allegra CJ. Autoregulation of human thymidylate synthase messenger RNA translation by thymidylate synthase. Proc Natl Acad Sci USA. 1991;88(20):8977-81.
13. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-97.
14. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120(1):15-20.
15. Verghese ET, Hanby AM, Speirs V, Hughes TA. Small is beautiful: microRNAs and breast cancer-where are we now? J Pathol. 2008;215(3):214-21.
16. Wang F, Li T, Zhang B, Li H, Wu Q, Yang L, Nie Y, Wu K, Shi Y, Fan D. MicroRNA-19a/b regulates multidrug resistance in human gastric cancer cells by targeting PTEN. Biochem biophys Res Commun. 2013;434(3):688-94.
17. Bockhorn J, Dalton R, Nwachukwu C, Huang S, Prat A, Yee K, Chang YF, Huo D, Wen Y, Swanson KE, et al. MicroRNA-30c inhibits human breast tumour chemotherapy resistance by regulating TWF1 and IL-11. Nature Commun. 2013;4:1393.
18. Zhang Y, Lu Q, Cai X. MicroRNA-106a induces multidrug resistance in gastric cancer by targeting RUNX3. FEBS Lett. 2013;587(18):3069-75.
19. Zhou Y, Huang Z, Wu S, Zang X, Liu M, Shi J. miR-33a is up-regulated in chemoresistant osteosarcoma and promotes osteosarcoma cell resistance to cisplatin by down-regulating TWIST. J Exp Clinical Cancer Res CR. 2014;33:12.
20. Lv L, Deng H, Li Y, Zhang C, Liu X, Liu Q, Zhang D, Wang L, Pu Y, Zhang H, et al. The DNA methylation-regulated miR-193a-3p dictates the multi-chemoresistance of bladder cancer via repression of SRSF2/PLAU/HIC2 expression. Cell Death Dis. 2014;5:e1402.
21. Tarazona S, Garcia-Alcalde F, Dopazo J, Ferrer A, Conesa A. Differential expression in RNA-seq: a matter of depth. Genome Res. 2011;21(12):2213-23.
22. Lv L, Deng H, Li Y, Zhang C, Liu X, Liu Q, Zhang D, Wang L, Pu Y, Zhang H, He Y, Wang Y, Yu Y, Yu T, Zhu J. The DNA methylation-regulated miR-193a-3p dictates the multi-chemoresistance of bladder cancer via repression of SRSF2/PLAU/HIC2 expression. Cell Death Dis. 2014;5:e1402.
23. Heiser LM, Sadanandam A, Kuo WL, Benz SC, Goldstein TC, Ng S, Gibb WJ, Wang NJ, Ziyad S, Tong F, et al. Subtype and pathway specific responses to anticancer compounds in breast cancer. Proc Natl Acad Sci USA. 2012;109(8):2724-9.
24. Andrisano V, Bartolini M, Gotti R, Cavrini V, Felix G. Determination of inhibitors' potency (IC50) by a direct high-performance liquid chromatographic method on an immobilised acetylcholinesterase column. J Chromatogr B Biomed Sci Appl. 2001;753(2):375-83.
25. Pu Y, Zhao F, Wang H, Cai W, Gao J, Li Y, Cai S. MiR-34a-5p promotes the multi-drug resistance of osteosarcoma by targeting the CD117 gene. Oncotarget. 2016.
26. Zhu Y, Tian F, Li H, Zhou Y, Lu J, Ge Q. Profiling maternal plasma microRNA expression in early pregnancy to predict gestational diabetes mellitus. Int J Gynaecol Obstetr. 2015;130:49-53.
27. Wen Y, Han J, Chen J, Dong J, Xia Y, Liu J, Jiang Y, Dai J, Lu J, Jin G, et al. Plasma miRNAs as early biomarkers for detecting hepatocellular carcinoma. Int J Cancer. 2015;137:1679-90.
28. Honegger A, Schilling D, Bastian S, Sponagel J, Kuryshev V, Sultmann H, Scheffner M, Hoppe-Seyler K, Hoppe-Seyler F. Dependence of intracellular and exosomal microRNAs on viral E6/E7 oncogene expression in HPV-positive tumor cells. PLoS Pathog. 2015;11(3):e1004712.
29. Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R. The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes. 2014;5(5):675-80.
30. Zhi F, Shao N, Wang R, Deng D, Xue L, Wang Q, Zhang Y, Shi Y, Xia X, Wang S, et al. Identification of 9 serum microRNAs as potential noninvasive biomarkers of human astrocytoma. Neuro-oncology. 2014;17:383-91.
31. Agrawal R, Pandey P, Jha P, Dwivedi V, Sarkar C, Kulshreshtha R. Hypoxic signature of microRNAs in glioblastoma: insights from small RNA deep sequencing. BMC Genom. 2014;15:686.
32. Ye SB, Li ZL, Luo DH, Huang BJ, Chen YS, Zhang XS, Cui J, Zeng YX, Li J. Tumor-derived exosomes promote tumor progression and T-cell dysfunction through the regulation of enriched exosomal microRNAs in human nasopharyngeal carcinoma. Oncotarget. 2014;5(14):5439-52.
33. Calvano Filho CM, Calvano-Mendes DC, Carvalho KC, Maciel GA, Ricci MD, Torres AP, Filassi JR, Baracat EC, , Triple-negative and luminal A breast tumors: differential expression of miR-18a-5p, miR-17-5p, and miR-20a-5p. Tumour Biol. 2014;35(8):7733-41.
34. Leung CM, Chen TW, Li SC, Ho MR, Hu LY, Liu WS, Wu TT, Hsu PC, Chang HT, Tsai KW. MicroRNA expression profiles in human breast cancer cells after multifraction and single-dose radiation treatment. Oncol Rep. 2014;31(5):2147-56.
35. Xu Q, Dong QG, Sun LP, He CY, Yuan Y. Expression of serum miR-20a-5p, let-7a, and miR-320a and their correlations with pepsinogen in atrophic gastritis and gastric cancer: a case-control study. BMC Clin Pathol. 2013;13:11.
36. Sanfiorenzo C, Ilie MI, Belaid A, Barlesi F, Mouroux J, Marquette CH, Brest P, Hofman P. Two panels of plasma microRNAs as non-invasive biomarkers for prediction of recurrence in resectable NSCLC. PLoS ONE. 2013;8(1):e54596.
37. Rath O, Kozielski F. Kinesins and cancer. Nat Rev Cancer. 2012;12(8):527-39.
38. Yu Y, Feng YM. The role of kinesin family proteins in tumorigenesis and progression: potential biomarkers and molecular targets for cancer therapy. Cancer. 2010;116(22):5150-60.
39. Marikawa Y, Fujita TC, Alarcon VB. An enhancer-trap LacZ transgene reveals a distinct expression pattern of Kinesin family 26B in mouse embryos. Dev Genes Evol. 2004;214(2):64-71.
40. Uchiyama Y, Sakaguchi M, Terabayashi T, Inenaga T, Inoue S, Kobayashi C, Oshima N, Kiyonari H, Nakagata N, Sato Y, et al. Kif26b, a kinesin family gene, regulates adhesion of the embryonic kidney mesenchyme. Proc Natl Acad Sci USA. 2010;107(20):9240-5.
41. Wang Q, Zhao ZB, Wang G, Hui Z, Wang MH, Pan JF, Zheng H. High expression of KIF26B in breast cancer associates with poor prognosis. PLoS ONE. 2013;8(4):e61640.
42. Gu J, Ajani JA, Hawk ET, Ye Y, Lee JH, Bhutani MS, Hofstetter WL, Swisher SG, Wang KK, Wu X. Genome-wide catalogue of chromosomal aberrations in barrett's esophagus and esophageal adenocarcinoma: a high-density single nucleotide polymorphism array analysis. Cancer Prev Res (Phila). 2010;3(9):1176-86.
43. Horpaopan S, Spier I, Zink AM, Altmuller J, Holzapfel S, Laner A, Vogt S, Uhlhaas S, Heilmann S, Stienen D, et al. Genome-wide CNV analysis in 221 unrelated patients and targeted high-throughput sequencing reveal novel causative candidate genes for colorectal adenomatous polyposis. Int J Cancer. 2015;136(6):E578-89.
44. Wang J, Cui F, Wang X, Xue Y, Chen J, Yu Y, Lu H, Zhang M, Tang H, Peng Z. Elevated kinesin family member 26B is a prognostic biomarker and a potential therapeutic target for colorectal cancer. J Exp Clin Cancer Res. 2015;34(1):13.
45. Axenovich SA, Kazarov AR, Boiko AD, Armin G, Roninson IB, Gudkov AV. Altered expression of ubiquitous kinesin heavy chain results in resistance to etoposide and hypersensitivity to colchicine: mapping of the domain associated with drug response. Cancer Res. 1998;58(15):3423-8.
46. Watters JW, Dewar K, Lehoczky J, Boyartchuk V, Dietrich WF. Kif1C, a kinesin-like motor protein, mediates mouse macrophage resistance to anthrax lethal factor. Curr Biol. 2001;11(19):1503-11.
47. De S, Cipriano R, Jackson MW, Stark GR. Overexpression of kinesins mediates docetaxel resistance in breast cancer cells. Cancer Res. 2009;69(20):8035-42.
48. Ganguly A, Yang H, Pedroza M, Bhattacharya R, Cabral F. Mitotic centromere-associated kinesin (MCAK) mediates paclitaxel resistance. J Biol Chem. 2011;286(42):36378-84.
49. Ganguly A, Yang H, Cabral F. Overexpression of mitotic centromere-associated Kinesin stimulates microtubule detachment and confers resistance to paclitaxel. Mol Cancer Ther. 2011;10(6):929-37.
50. Singel SM, Cornelius C, Zaganjor E, Batten K, Sarode VR, Buckley DL, Peng Y, John GB, Li HC, Sadeghi N, et al. KIF14 promotes AKT phosphorylation and contributes to chemoresistance in triple-negative breast cancer. Neoplasia. 2014;16(3):247-56.
51. Yin Y, Sun H, Xu J, Xiao F, Wang H, Yang Y, Ren H, Wu CT, Gao C, Wang L. Kinesin spindle protein inhibitor SB743921 induces mitotic arrest and apoptosis and overcomes imatinib resistance of chronic myeloid leukemia cells. Leuk Lymphoma. 2014;56:1813-20.
52. Huszar D, Theoclitou ME, Skolnik J, Herbst R. Kinesin motor proteins as targets for cancer therapy. Cancer Metastasis Rev. 2009;28(1-2):197-208.
53. Liu X, Gong H, Huang K. Oncogenic role of kinesin proteins and targeting kinesin therapy. Cancer Sci. 2013;104(6):651-6.
54. Jiang C, You Q. Kinesin spindle protein inhibitors in cancer: a patent review (2008-present). Expert Opin Ther Pat. 2013;23(12):1547-60.
55. Suzuki N, Hazama S, Ueno T, Matsui H, Shindo Y, Iida M, Yoshimura K, Yoshino S, Takeda K, Oka M. A phase I clinical trial of vaccination with KIF20A-derived peptide in combination with gemcitabine for patients with advanced pancreatic cancer. J Immunother. 2014;37(1):36-42.
56. Wood W, Jacinto A, Grose R, Woolner S, Gale J, Wilson C, Martin P. Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol. 2002;4(11):907-12.
57. Berg JS, Cheney RE. Myosin-X is an unconventional myosin that undergoes intrafilopodial motility. Nat Cell Biol. 2002;4(3):246-50.
58. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163-77.
59. Yu H, Wang N, Ju X, Yang Y, Sun D, Lai M, Cui L, Sheikh MA, Zhang J, Wang X, et al. PtdIns (3,4,5) P3 recruitment of Myo10 is essential for axon development. PLoS ONE. 2012;7(5):e36988.
60. Schoumacher M, Goldman RD, Louvard D, Vignjevic DM. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol. 2010;189(3):541-56.
61. Arjonen A, Kaukonen R, Mattila E, Rouhi P, Hognas G, Sihto H, Miller BW, Morton JP, Bucher E, Taimen P, et al. Mutant p53-associated myosin-X upregulation promotes breast cancer invasion and metastasis. J Clin Investig. 2014;124(3):1069-82.
62. Cao R, Chen J, Zhang X, Zhai Y, Qing X, Xing W, Zhang L, Malik YS, Yu H, Zhu X. Elevated expression of myosin X in tumours contributes to breast cancer aggressiveness and metastasis. Br J Cancer. 2014;111(3):539-50.
63. Huggon IC, Davies A, Gove C, Moscoso G, Moniz C, Foss Y, Farzaneh F, Towner P. Molecular cloning of human GATA-6 DNA binding protein: high levels of expression in heart and gut. Biochim Biophys Acta. 1997;1353(2):98-102.
64. Budovskaya YV, Wu K, Southworth LK, Jiang M, Tedesco P, Johnson TE, Kim SK. An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell. 2008;134(2):291-303.
65. Burch JB. Regulation of GATA gene expression during vertebrate development. Semin Cell Dev Biol. 2005;16(1):71-81.
66. Kwei KA, Bashyam MD, Kao J, Ratheesh R, Reddy EC, Kim YH, Montgomery K, Giacomini CP, Choi YL, Chatterjee S, et al. Genomic profiling identifies GATA6 as a candidate oncogene amplified in pancreatobiliary cancer. PLoS Genet. 2008;4(5):e1000081.
67. Fu B, Luo M, Lakkur S, Lucito R, Iacobuzio-Donahue CA. Frequent genomic copy number gain and overexpression of GATA-6 in pancreatic carcinoma. Cancer Biol Ther. 2008;7(10):1593-601.
68. Al-azzeh ED, Fegert P, Blin N, Gott P. Transcription factor GATA-6 activates expression of gastroprotective trefoil genes TFF1 and TFF2. Biochim Biophys Acta. 2000;1490(3):324-32.
69. Akiyama Y, Watkins N, Suzuki H, Jair KW, van Engeland M, Esteller M, Sakai H, Ren CY, Yuasa Y, Herman JG, et al. GATA-4 and GATA-5 transcription factor genes and potential downstream antitumor target genes are epigenetically silenced in colorectal and gastric cancer. Mol Cell Biol. 2003;23(23):8429-39.
70. Guo M, Akiyama Y, House MG, Hooker CM, Heath E, Gabrielson E, Yang SC, Han Y, Baylin SB, Herman JG, et al. Hypermethylation of the GATA genes in lung cancer. Clin Cancer Res. 2004;10(23):7917-24.
71. Lin L, Bass AJ, Lockwood WW, Wang Z, Silvers AL, Thomas DG, Chang AC, Lin J, Orringer MB, Li W, et al. Activation of GATA binding protein 6 (GATA6) sustains oncogenic lineage-survival in esophageal adenocarcinoma. Proc Natl Acad Sci USA. 2012;109(11):4251-6.
72. Rong L, Liu J, Qi Y, Graham AM, Parmacek MS, Li S. GATA-6 promotes cell survival by up-regulating BMP-2 expression during embryonic stem cell differentiation. Mol Biol Cell. 2012;23(18):3754-63.
73. Shureiqi I, Jiang W, Fischer SM, Xu X, Chen D, Lee JJ, Lotan R, Lippman SM. GATA-6 transcriptional regulation of 15-lipoxygenase-1 during NSAID-induced apoptosis in colorectal cancer cells. Cancer Res. 2002;62(4):1178-83.
74. Shureiqi I, Zuo X, Broaddus R, Wu Y, Guan B, Morris JS, Lippman SM. The transcription factor GATA-6 is overexpressed in vivo and contributes to silencing 15-LOX-1 in vitro in human colon cancer. FASEB J. 2007;21(3):743-53.