miR-203 induces oxaliplatin resistance in colorectal cancer cells by negatively regulating ATM kinase

Molecular Oncology

Volumn 8, Issue 1, 2014, Pages 83-92

  Zhou, Yunfei ^a   Wan, Guohui ^a   Spizzo, Riccardo ^a   Ivan, Cristina ^a   Mathur, Rohit ^a   Hu, Xiaoxiao ^a   Ye, Xiangcang ^a   Lu, Jia ^a   Fan, Fan ^a   Xia, Ling ^a   Calin, George A ^a   Ellis, Lee M ^a   Lu, Xiongbin ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

ATM; Chemoresistance; DNA damage response; MiR 203; Oxaliplatin

Indexed keywords

ATM PROTEIN; MESSENGER RNA; MICRORNA; MICRORNA 203; OXALIPLATIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CANCER ADJUVANT THERAPY; CANCER CELL; CANCER RESISTANCE; CANCER RISK; COLORECTAL CANCER; COMPUTER MODEL; CONTROLLED STUDY; DATA BASE; DNA DAMAGE; DOWN REGULATION; ENZYME REGULATION; GENE EXPRESSION; GENE TARGETING; HEALTH CARE QUALITY; HUMAN; HUMAN CELL; MEDIATOR RELEASE; METASTATIC COLORECTAL CANCER; PRIORITY JOURNAL; UNTRANSLATED REGION; UPREGULATION;

ATAXIA TELANGIECTASIA;

ATM; CHEMORESISTANCE; DNA DAMAGE RESPONSE; MIR-203; OXALIPLATIN;

ANTINEOPLASTIC AGENTS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; COLON; COLORECTAL NEOPLASMS; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICRORNAS; ORGANOPLATINUM COMPOUNDS; RECTUM;

EID: 84892963069     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.09.004     Document Type: Article

References (51)

1. Ahmad S. Platinum-DNA interactions and subsequent cellular processes controlling sensitivity to anticancer platinum complexes. Chem. Biodiversity 2010, 7:543-566.
2. Alberts S.R., Horvath W.L., Sternfeld W.C., Goldberg R.M., Mahoney M.R., Dakhil S.R., Levitt R., Rowland K., Nair S., Sargent D.J., Donohue J.H. Oxaliplatin, fluorouracil, and leucovorin for patients with unresectable liver-only metastases from colorectal cancer: a North Central Cancer Treatment Group phase II study. J. Clin. Oncol. Official J. Am. Soc. Clin. Oncol. 2005, 23:9243-9249.
3. Andre T., Boni C., Mounedji-Boudiaf L., Navarro M., Tabernero J., Hickish T., Topham C., Zaninelli M., Clingan P., Bridgewater J., Tabah-Fisch I., de Gramont A. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N. Engl. J. Med. 2004, 350:2343-2351.
4. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870.
5. Boll K., Reiche K., Kasack K., Morbt N., Kretzschmar A.K., Tomm J.M., Verhaegh G., Schalken J., von Bergen M., Horn F., Hackermuller J. MiR-130a, miR-203 and miR-205 jointly repress key oncogenic pathways and are downregulated in prostate carcinoma. Oncogene 2013, 32:277-285.
6. Bose D., Zimmerman L.J., Pierobon M., Petricoin E., Tozzi F., Parikh A., Fan F., Dallas N., Xia L., Gaur P., Samuel S., Liebler D.C., Ellis L.M. Chemoresistant colorectal cancer cells and cancer stem cells mediate growth and survival of bystander cells. Br. J. Cancer. 2011, 105:1759-1767.
7. Calin G.A., Sevignani C., Dumitru C.D., Hyslop T., Noch E., Yendamuri S., Shimizu M., Rattan S., Bullrich F., Negrini M., Croce C.M. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. U S A 2004, 101:2999-3004.
8. Cassidy J., Clarke S., Diaz-Rubio E., Scheithauer W., Figer A., Wong R., Koski S., Lichinitser M., Yang T.S., Rivera F., Couture F., Sirzen F., Saltz L. Randomized phase III study of capecitabine plus oxaliplatin compared with fluorouracil/folinic acid plus oxaliplatin as first-line therapy for metastatic colorectal cancer. J. Clin. Oncol. Official J. Am. Soc. Clin. Oncol. 2008, 26:2006-2012.
9. Chen L., Tang Y., Wang J., Yan Z., Xu R. miR-421 induces cell proliferation and apoptosis resistance in human nasopharyngeal carcinoma via downregulation of FOXO4. Biochem. Biophys. Res. Commun. 2013, 435:745-750.
10. Dai Z., Huang Y., Sadee W. Growth factor signaling and resistance to cancer chemotherapy. Curr. Top. Med. Chem. 2004, 4:1347-1356.
11. Dallas N.A., Xia L., Fan F., Gray M.J., Gaur P., van Buren G., Samuel S., Kim M.P., Lim S.J., Ellis L.M. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res. 2009, 69:1951-1957.
12. Davies J.M., Goldberg R.M. First-line therapeutic strategies in metastatic colorectal cancer. Oncol. (Williston Park, N.Y) 2008, 22:1470-1479.
13. Fish J.E., Santoro M.M., Morton S.U., Yu S., Yeh R.F., Wythe J.D., Ivey K.N., Bruneau B.G., Stainier D.Y., Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Develop. Dev. Cell.Cell 2008, 15:272-284.
14. Gilbert L.A., Hemann M.T. DNA damage-mediated induction of a chemoresistant niche. Cell 2010, 143:355-366.
15. Goldberg R.M., Sargent D.J., Morton R.F., Fuchs C.S., Ramanathan R.K., Williamson S.K., Findlay B.P., Pitot H.C., Alberts S.R. A randomized controlled trial of fluorouracil plus leucovorin, irinotecan, and oxaliplatin combinations in patients with previously untreated metastatic colorectal cancer. J. Clin. Oncol. Official J. Am. Soc. Clin. Oncol. 2004, 22:23-30.
16. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio R.A., Kastrinakis N.G., Levy B., Kletsas D., Yoneta A., Herlyn M., Kittas C., Halazonetis T.D. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434:907-913.
17. Gottardo F., Liu C.G., Ferracin M., Calin G.A., Fassan M., Bassi P., Sevignani C., Byrne D., Negrini M., Pagano F., Gomella L.G., Croce C.M., Baffa R. Micro-RNA profiling in kidney and bladder cancers. Urologic. Oncol. 2007, 25:387-392.
18. Gourdier I., Del Rio M., Crabbe L., Candeil L., Copois V., Ychou M., Auffray C., Martineau P., Mechti N., Pommier Y., Pau B. Drug specific resistance to oxaliplatin is associated with apoptosis defect in a cellular model of colon carcinoma. FEBS Lett. 2002, 529:232-236.
19. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., Vadas M.A., Khew-Goodall Y., Goodall G.J. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell. Biol. 2008, 10:593-601.
20. Gregory P.A., Bracken C.P., Smith E., Bert A.G., Wright J.A., Roslan S., Morris M., Wyatt L., Farshid G., Lim Y.Y., Lindeman G.J., Shannon M.F., Drew P.A., Khew-Goodall Y., Goodall G.J. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol. Biol. Cell 2011, 22:1686-1698.
21. Greither T., Grochola L.F., Udelnow A., Lautenschlager C., Wurl P., Taubert H. Elevated expression of microRNAs 155, 203, 210 and 222 in pancreatic tumors is associated with poorer survival. Int. J. Cancer 2010, 126:73-80.
22. Hector S., Bolanowska-Higdon W., Zdanowicz J., Hitt S., Pendyala L. In vitro studies on the mechanisms of oxaliplatin resistance. Cancer. Chemother. Pharmacol. 2001, 48:398-406.
23. Huang W.C., Hung M.C. Induction of Akt activity by chemotherapy confers acquired resistance. J. Formos. Medical Assoc. - Taiwan yi zhi 2009, 108:180-194.
24. Iorio M.V., Visone R., Di Leva G., Donati V., Petrocca F., Casalini P., Taccioli C., Volinia S., Liu C.G., Alder H., Calin G.A., Menard S., Croce C.M. MicroRNA signatures in human ovarian cancer. Cancer Res. 2007, 67:8699-8707.
25. Jackson S.J., Zhang Z., Feng D., Flagg M., O'Loughlin E., Wang D., Stokes N., Fuchs E., Yi R. Rapid and widespread suppression of self-renewal by microRNA-203 during epidermal differentiation. Development 2013, 140:1882-1891.
26. Jordan M.A., Wilson L. Microtubules as a target for anticancer drugs. Nat. Rev. Cancer. 2004, 4:253-265.
27. Lal A., Pan Y., Navarro F., Dykxhoorn D.M., Moreau L., Meire E., Bentwich Z., Lieberman J., Chowdhury D. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nature Struct. Mol. Biol. 2009, 16:492-498.
28. Landriscina M., Maddalena F., Laudiero G., Esposito F. Adaptation to oxidative stress, chemoresistance, and cell survival. Antioxid. Redox. Signal. 2009, 11:2701-2716.
29. Li J., Chen Y., Zhao J., Kong F., Zhang Y. miR-203 reverses chemoresistance in p53-mutated colon cancer cells through downregulation of Akt2 expression. Cancer. Lett. 2011, 304:52-59.
30. Liu C.G., Calin G.A., Volinia S., Croce C.M. MicroRNA expression profiling using microarrays. Nature Protocol. 2008, 3:563-578.
31. Mathe E.A., Nguyen G.H., Bowman E.D., Zhao Y., Budhu A., Schetter A.J., Braun R., Reimers M., Kumamoto K., Hughes D., Altorki N.K., Casson A.G., Liu C.G., Wang X.W., Yanaihara N., Hagiwara N., Dannenberg A.J., Miyashita M., Croce C.M., Harris C.C. MicroRNA expression in squamous cell carcinoma and adenocarcinoma of the esophagus: associations with survival. Clin Cancer Res. 2009, 15:6192-6200.
32. Meyerhardt J.A., Mayer R.J. Systemic therapy for colorectal cancer. N. Engl. J. Med. 2005, 352:476-487.
33. Network C.G.A. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012, 487:330-337.
34. Noguchi S., Mori T., Otsuka Y., Yamada N., Yasui Y., Iwasaki J., Kumazaki M., Maruo K., Akao Y. Anti-oncogenic microRNA-203 induces senescence by targeting E2F3 protein in human melanoma cells. J. Biol. Chem. 2012, 287:11769-11777.
35. Sau A., Pellizzari Tregno F., Valentino F., Federici G., Caccuri A.M. Glutathione transferases and development of new principles to overcome drug resistance. Arch. Biochem. Biophys. 2010, 500:116-122.
36. Schetter A.J., Leung S.Y., Sohn J.J., Zanetti K.A., Bowman E.D., Yanaihara N., Yuen S.T., Chan T.L., Kwong D.L., Au G.K., Liu C.G., Calin G.A., Croce C.M., Harris C.C. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. Jama 2008, 299:425-436.
37. Spizzo R., Nicoloso M.S., Croce C.M., Calin G.A. SnapShot: MicroRNAs in cancer. Cell 2009, 137:586. e581.
38. Tokarz P., Blasiak J. The role of MiRNA in metastatic colorectal cancer and its significance in cancer prognosis and treatment. Acta. Biochim. Pol. 2012, 59:467-474.
39. Viticchie G., Lena A.M., Cianfarani F., Odorisio T., Annicchiarico-Petruzzelli M., Melino G., Candi E. MicroRNA-203 contributes to skin re-epithelialization. Cell Death Dis. 2012, 3:e435.
40. Viticchie G., Lena A.M., Latina A., Formosa A., Gregersen L.H., Lund A.H., Bernardini S., Mauriello A., Miano R., Spagnoli L.G., Knight R.A., Candi E., Melino G. MiR-203 controls proliferation, migration and invasive potential of prostate cancer cell lines. Cell Cycle 2011, 10:1121-1131.
41. 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, 103:2257-2261.
42. Wan G., Zhang X., Langley R.R., Liu Y., Hu X., Han C., Peng G., Ellis L.M., Jones S.N., Lu X. DNA-damage-induced nuclear export of precursor microRNAs is regulated by the ATM-AKT pathway. Cell Rep 2013, 3:2100-2112.
43. Wang D., Lippard S.J. Cellular processing of platinum anticancer drugs. Nat. Rev. Drug. Discov. 2005, 4:307-320.
44. Yang A.D., Fan F., Camp E.R., van Buren G., Liu W., Somcio R., Gray M.J., Cheng H., Hoff P.M., Ellis L.M. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res. 2006, 12:4147-4153.
45. Yang S.Y., Sales K.M., Fuller B., Seifalian A.M., Winslet M.C. Apoptosis and colorectal cancer: implications for therapy. Trends. Mol. Med. 2009, 15:225-233.
46. Yi R., Poy M.N., Stoffel M., Fuchs E. A skin microRNA promotes differentiation by repressing 'stemness'. Nature 2008, 452:225-229.
47. Zhai H., Fesler A., Ju J. MicroRNA: a third dimension in autophagy. Cell Cycle 2012, 12.
48. Zhai H., Ju J. Implications of microRNAs in colorectal cancer development, diagnosis, prognosis, and therapeutics. Front. Genet. 2011, 2.
49. Zhang X., Wan G., Berger F.G., He X., Lu X. The ATM kinase induces microRNA biogenesis in the DNA damage response. Mol. Cell 2011, 41:371-383.
50. Zhao S., Yao D.S., Chen J.Y., Ding N. Aberrant expression of miR-20a and miR-203 in cervical cancer. Asian Pac. J. Cancer Prevent.: APJCP 2013, 14:2289-2293.
51. Zhou Y., Tozzi F., Chen J., Fan F., Xia L., Wang J., Gao G., Zhang A., Xia X., Brasher H., Widger W., Ellis L.M., Weihua Z. Intracellular ATP levels are a pivotal determinant of chemoresistance in colon cancer cells. Cancer Res. 2012, 72:304-314.