MiR-135a contributes to paclitaxel resistance in tumor cells both in vitro and in vivo

Oncogene

Volumn 30, Issue 43, 2011, Pages 4386-4398

  Holleman, A ^a,b   Chung, I ^a   Olsen, R R ^a   Kwak, B ^a   Mizokami, A ^c   Saijo, N ^d   Parissenti, A ^e   Duan, Z ^f   Voest, E E ^g   Zetter, B R ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MEANDER MEDICAL CENTER   (Netherlands)

^c KANAZAWA UNIVERSITY   (Japan)

^d NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^e SUDBURY REGIONAL HOSPITAL   (Canada)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g Utrecht Medical Center   (Netherlands)

Author keywords

APC; carcinoma; miRNA 135a; paclitaxel resistance

Indexed keywords

APC PROTEIN; MICRORNA; PACLITAXEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CONTROLLED STUDY; DRUG RESPONSE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETRANSPLANTATION; TUMOR CELL LINE; UPREGULATION;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, APC; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; MICRORNAS; NEOPLASM TRANSPLANTATION; PACLITAXEL; UP-REGULATION;

MUS;

EID: 80055026409     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.148     Document Type: Article

References (54)

1. Anand S, Penrhyn-Lowe S, Venkitaraman AR. (2003). AURORA-A amplification overrides the mitotic spindle assembly checkpoint, inducing resistance to Taxol. Cancer Cell 3: 51-62. (Pubitemid 37443890)
2. Aoki K, Taketo MM. (2007). Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J Cell Sci 120: 3327-3335. (Pubitemid 350028340)
3. Blower PE, Verducci JS, Lin S, Zhou J, Chung JH, Dai Z et al. (2007). MicroRNA expression profiles for the NCI-60 cancer cell panel. Mol Cancer Ther 6: 1483-1491. (Pubitemid 46954015)
4. Chu Q, Vincent M, Logan D, Mackay JA, Evans WK. (2005). Taxanes as first-line therapy for advanced non-small cell lung cancer: a systematic review and practice guideline. Lung Cancer 50: 355-374.
5. Cleveland WS. (1979). Robust locally weighted regression and smoothing scatter plots. J Amer Statist Assoc 74: 829-836.
6. Cochrane DR, Spoelstra NS, Howe EN, Nordeen SK, Richer JK. (2009). MicroRNA-200c mitigates invasiveness and restores sensitivity to microtubule-targeting chemotherapeutic agents. Mol Cancer Ther 8: 1055-1066.
7. Dikovskaya D, Schiffmann D, Newton IP, Oakley A, Kroboth K, Sansom O et al. (2007). Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J Cell Biol 176: 183-195. (Pubitemid 46143259)
8. Dombernowsky P, Gehl J, Boesgaard M, Paaske T, Jensen BV. (1996). Doxorubicin and paclitaxel, a highly active combination in the treatment of metastatic breast cancer. Semin Oncol 23: 23-27. (Pubitemid 26362181)
9. Esquela-Kerscher A, Slack FJ. (2006). Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269.
10. Fodde R, Kuipers J, Rosenberg C, Smits R, Kielman M, Gaspar C et al. (2001). Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 3: 433-438. (Pubitemid 32288454)
11. Fong GH. (2008). Mechanisms of adaptive angiogenesis to tissue hypoxia. Angiogenesis 11: 121-140.
12. Fujita Y, Kojima K, Ohhashi R, Hamada N, Nozawa Y, Kitamoto A et al. (2010). MiR-148a attenuates paclitaxel-resistance of hormonerefractory, drug-resistant prostate cancer PC3 cells by regulating MSK1 expression. J Biol Chem 25: 19076-19084.
13. Gelfand VI, Bershadsky AD. (1991). Microtubule dynamics: mechanism, regulation, and function. Annu Rev Cell Biol 7: 93-116.
14. Giles RH, van Es JH, Clevers H. (2003). Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta 1653: 1-24. (Pubitemid 36627817)
15. Goldie JH, Coldman AJ. (1979). A mathematic model for relating the drug sensitivity of tumors to their spontaneous mutation rate. Cancer Treat Rep 63: 1727-1733. (Pubitemid 10138923)
16. Greenberger LM, Lothstein L, Williams SS, Horwitz SB. (1988). Distinct P-glycoprotein precursors are overproduced in independently isolated drug-resistant cell lines. Proc Natl Acad Sci USA 85: 3762-3766.
17. Haldar S, Chintapalli J, Croce CM. (1996). Taxol induces bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res 56: 1253-1255. (Pubitemid 26080965)
18. He L, Hannon GJ. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531. (Pubitemid 38868508)
19. Hoffman RM. (1991). Three-dimensional histoculture: origins and applications in cancer research. Cancer Cells 3: 86-92.
20. Huang G, Chen L. (2010). Recombinant human endostatin improves anti-tumor efficacy of paclitaxel by normalizing tumor vasculature in Lewis lung carcinoma. J Cancer Res Clin Oncol 136: 1201-1211.
21. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S et al. (2005). MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070. (Pubitemid 41161233)
22. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS. (2001). A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 3: 429-432. (Pubitemid 32288453)
23. Kobayashi H, Man S, Graham CH, Kapitain SJ, Teicher BA, Kerbel RS. (1993). Acquired multicellular-mediated resistance to alkylating agents in cancer. Proc Natl Acad Sci USA 90: 3294-3298. (Pubitemid 23111352)
24. Kovalchuk O, Filkowski J, Meservy J, Ilnytskyy Y, Tryndyak VP, Chekhun VF et al. (2008). Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther 7: 2152-2159.
25. Lepourcelet M, Chen YN, France DS, Wang H, Crews P, Petersen F et al. (2004). Small-molecule antagonists of the oncogenic Tcf/betacatenin protein complex. Cancer Cell 5: 91-102. (Pubitemid 38121599)
26. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D et al. (2005). MicroRNA expression profiles classify human cancers. Nature 435: 834-838. (Pubitemid 40839735)
27. Mackler NJ, Pienta KJ. (2005). Drug insight: use of docetaxel in prostate and urothelial cancers. Nat Clin Pract Urol 2: 92-100. (Pubitemid 40790129)
28. Mahon PC, Hirota K, Semenza GL. (2001). FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev 15: 2675-2686. (Pubitemid 32988878)
29. McGrogan BT, Gilmartin B, Carney DN, McCann A. (2008). Taxanes, microtubules and chemoresistant breast cancer. Biochim Biophys Acta 1785: 96-132.
30. Meads MB, Gatenby RA, Dalton WS. (2009). Environment-mediated drug resistance: a major contributor to minimal residual disease. Nat Rev Cancer 9: 665-674.
31. Mercatelli N, Coppola V, Bonci D, Miele F, Costantini A, Guadagnoli M et al. (2008). The inhibition of the highly expressed miR-221 and miR-222 impairs the growth of prostate carcinoma xenografts in mice. PLoS ONE 3: e4029.
32. Mozzetti S, Ferlini C, Concolino P, Filippetti F, Raspaglio G, Prislei S et al. (2005). Class III beta-tubulin overexpression is a prominent mechanism of paclitaxel resistance in ovarian cancer patients. Clin Cancer Res 11: 298-305. (Pubitemid 40075808)
33. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink JA, Bolijn A et al. (2008). Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 68: 5795-5802.
34. Oguri T, Ozasa H, Uemura T, Bessho Y, Miyazaki M, Maeno K et al. (2008). MRP7/ABCC10 expression is a predictive biomarker for the resistance to paclitaxel in non-small cell lung cancer. Mol Cancer Ther 7: 1150-1155.
35. Okugawa K, Kobayashi H, Hirakawa T, Sonoda T, Ogura T, Nakano H. (2004). In vivo establishment and characterization of a paclitaxelresistant human ovarian cancer cell line showing enhanced growth properties and drug-resistance only in vivo. J Cancer Res Clin Oncol 130: 178-186. (Pubitemid 38392351)
36. Patel N, Chatterjee SK, Vrbanac V, Chung I, Mu CJ, Olsen RR et al. (2010). Rescue of paclitaxel sensitivity by repression of Prohibitin1 in drug-resistant cancer cells. Proc Natl Acad Sci USA 107: 2503-2508.
37. Perkins C, Kim CN, Fang G, Bhalla KN. (1998). Overexpression of Apaf-1 promotes apoptosis of untreated and paclitaxel- or etoposide- treated HL-60 cells. Cancer Res 58: 4561-4566. (Pubitemid 28480614)
38. Pollard JW. (2004). Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4: 71-78. (Pubitemid 38082155)
39. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A et al. (2007). A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700-2707. (Pubitemid 350048334)
40. Rottenberg S, Nygren AO, Pajic M, van Leeuwen FW, van der Heijden I, van de Wetering K et al. (2007). Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer. Proc Natl Acad Sci USA 104: 12117-12122. (Pubitemid 47185639)
41. Schiff PB, Fant J, Horwitz SB. (1979). Promotion of microtubule assembly in vitro by taxol. Nature 277: 665-667. (Pubitemid 9114288)
42. Shi J, Orth JD, Mitchison T. (2008). Cell type variation in responses to antimitotic drugs that target microtubules and kinesin-5. Cancer Res 68: 3269-3276.
43. Sorrentino A, Liu CG, Addario A, Peschle C, Scambia G, Ferlini C. (2008). Role of microRNAs in drug-resistant ovarian cancer cells. Gynecol Oncol 111: 478-486.
44. Starling JJ, Maciak RS, Hinson NA, Hoskins J, Laguzza BC, Gadski RA et al. (1990). in vivo selection of human tumor cells resistant to monoclonal antibody-Vinca alkaloid immunoconjugates. Cancer Res 50: 7634-7640.
45. Sudo T, Nitta M, Saya H, Ueno NT. (2004). Dependence of paclitaxel sensitivity on a functional spindle assembly checkpoint. Cancer Res 64: 2502-2508. (Pubitemid 38523906)
46. Takeda M, Mizokami A, Mamiya K, Li YQ, Zhang J, Keller ET et al. (2007). The establishment of two paclitaxel-resistant prostate cancer cell lines and the mechanisms of paclitaxel resistance with two cell lines. Prostate 67: 955-967. (Pubitemid 46828929)
47. Teicher BA, Herman TS, Holden SA, Wang YY, Pfeffer MR, Crawford JW et al. (1990). Tumor resistance to alkylating agents conferred by mechanisms operative only in vivo. Science 247: 1457-1461.
48. Villeneuve DJ, Hembruff SL, Veitch Z, Cecchetto M, Dew WA, Parissenti AM. (2006). cDNA microarray analysis of isogenic paclitaxel- and doxorubicin-resistant breast tumor cell lines reveals distinct drug-specific genetic signatures of resistance. Breast Cancer Res Treat 96: 17-39.
49. Wakelee H, Ramalingam S, Belani CP. (2005). Docetaxel in advanced non-small cell lung cancer. Expert Rev Anticancer Ther 5: 13-24. (Pubitemid 40287432)
50. Xia L, Zhang D, Du R, Pan Y, Zhao L, Sun S et al. (2008). miR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int J Cancer 123: 372-379. (Pubitemid 351842022)
51. Xie X, Lu J, Kulbokas EJ, Golub TR, Mootha V, Lindblad-Toh K et al. (2005). Systematic discovery of regulatory motifs in human promoters and 30 UTRs by comparison of several mammals. Nature 434: 338-345. (Pubitemid 40469170)
52. Yang YH, Speed T. (2002). Design issues for cDNA microarray experiments. Nat Rev Genet 3: 579-588. (Pubitemid 34827132)
53. Zhang T, Otevrel T, Gao Z, Ehrlich SM, Fields JZ, Boman BM. (2001). Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 61: 8664-8667. (Pubitemid 34013874)
54. Zhou M, Liu Z, Zhao Y, Ding Y, Liu H, Xi Y et al. (2010). MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist killer 1 (Bak1). J Biol Chem 285: 21496-21507.