MiR-193a-3p functions as a tumor suppressor in lung cancer by down-regulating ERBB4

Journal of Biological Chemistry

Volumn 290, Issue 2, 2015, Pages 926-940

  Liang, Hongwei ^a   Liu, Minghui ^a   Yan, Xin ^a   Zhou, Yong ^a   Wang, Wengong ^a   Wang, Xueliang ^a   Fu, Zheng ^a   Wang, Nan ^a   Zhang, Suyang ^a   Wang, Yanbo ^a   Zen, Ke ^a   Zhang, Chen Yu ^a   Hou, Dongxia ^a   Li, Jing ^a   Chen, Xi ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; CELL DEATH; TUMORS;

ANTITUMOR EFFECT; LUNG CANCER; LUNG CANCER CELLS; LUNG CANCER THERAPY; P-FUNCTION; TUMOR SUPPRESSORS;

DISEASES;

EPIDERMAL GROWTH FACTOR RECEPTOR 4; MICRORNA; MICRORNA 193A 3P; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ERBB4 PROTEIN, HUMAN; MIRN193 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BIOINFORMATICS; CANCER INHIBITION; CELL GROWTH; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC CORRELATION; GENETIC TRANSCRIPTION; GROWTH RATE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER CELL LINE; MALE; MIDDLE AGED; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; BIOSYNTHESIS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; PATHOLOGY; PROTEIN SYNTHESIS; TUMOR CELL LINE;

MUS;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MICE; MICRORNAS; PROTEIN BIOSYNTHESIS; RECEPTOR, ERBB-4; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84920973120     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.621409     Document Type: Article

References (56)

1. Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E., and Forman, D. (2011) Global cancer statistics. CA Cancer J. Clin. 61, 69-90
2. Ramalingam, S. S., Owonikoko, T. K., and Khuri, F. R. (2011) Lung cancer: new biological insights and recent therapeutic advances. CA Cancer J. Clin. 61, 91-112
3. Heist, R. S., and Engelman, J. A. (2012) SnapShot: non-small cell lung cancer. Cancer Cell 21, 448 e442
4. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
5. Zochbauer-Muller, S., Gazdar, A. F., and Minna, J. D. (2002) Molecular pathogenesis of lung cancer. Annu. Rev. Physiol. 64, 681-708
6. Harpole, D. H., Jr., Marks, J. R., Richards, W. G., Herndon, J. E., 2nd, and Sugarbaker, D. J. (1995) Localized adenocarcinoma of the lung: oncogene expression of erbB-2 and p53 in 150 patients. Clin. Cancer Res. 1, 659-664
7. Schneider, P. M., Praeuer, H. W., Stoeltzing, O., Boehm, J., Manning, J., Metzger, R., Fink, U., Wegerer, S., Hoelscher, A. H., and Roth, J. A. (2000) Multiple molecular marker testing (p53, C-Ki-ras, c-erbB-2) improves estimation of prognosis in potentially curative resected non-small cell lung cancer. Br. J. Cancer 83, 473-479
8. Bublil, E. M., and Yarden, Y. (2007) The EGF receptor family: spearheading a merger of signaling and therapeutics. Curr. Opin. Cell Biol. 19, 124-134
9. Furger, C., Fiddes, R. J., Quinn, D. I., Bova, R. J., Daly, R. J., and Sutherland, R. L. (1998) Granulosa cell tumors express erbB4 and are sensitive to the cytotoxic action of heregulin-2/PE40. Cancer Res. 58, 1773-1778
10. Gilmour, L. M., Macleod, K. G., McCaig, A., Gullick, W. J., Smyth, J. F., and Langdon, S. P. (2001) Expression of erbB-4/HER-4 growth factor receptor isoforms in ovarian cancer. Cancer Res. 61, 2169-2176
11. Graber, H. U., Friess, H., Kaufmann, B., Willi, D., Zimmermann, A., Korc, M., and Büchler, M. W. (1999) ErbB-4 mRNA expression is decreased in non-metastatic pancreatic cancer. Int. J. Cancer 84, 24-27
12. Haugen, D. R., Akslen, L. A., Varhaug, J. E., and Lillehaug, J. R. (1996) Expression of c-erbB-3 and c-erbB-4 proteins in papillary thyroid carcinomas. Cancer Res. 56, 1184-1188
13. Lyne, J. C., Melhem, M. F., Finley, G. G., Wen, D., Liu, N., Deng, D. H., and Salup, R. (1997) Tissue expression of neu differentiation factor/heregulin and its receptor complex in prostate cancer and its biologic effects on prostate cancer cells in vitro. Cancer J. Sci. Am. 3, 21-30
14. Merimsky, O., Staroselsky, A., Inbar, M., Schwartz, Y., Wigler, N., Mann, A., Marmor, S., and Greif, J. (2001) Correlation between c-erbB-4 receptor expression and response to gemcitabine-cisplatin chemotherapy in nonsmall-cell lung cancer. Ann. Oncol. 12, 1127-1131
15. Merimsky, O., Issakov, J., Bickels, J., Kollender, Y., Flusser, G., Soyfer, V., Schwartz, I., Inbar, M., and Meller, I. (2002) ErbB-4 expression in limb soft-tissue sarcoma: correlation with the results of neoadjuvant chemotherapy. Eur. J. Cancer 38, 1335-1342
16. Srinivasan, R., Benton, E., McCormick, F., Thomas, H., and Gullick, W. J. (1999) Expression of the c-erbB-3/HER-3 and c-erbB-4/HER-4 growth factor receptors and their ligands, neuregulin-1 -, neuregulin-1 -, and betacellulin, in normal endometrium and endometrial cancer. Clin. Cancer Res. 5, 2877-2883
17. Gilbertson, R. J., Perry, R. H., Kelly, P. J., Pearson, A. D., and Lunec, J. (1997) Prognostic significance of HER2 and HER4 coexpression in childhood medulloblastoma. Cancer Res. 57, 3272-3280
18. Gilbertson, R. J., Clifford, S. C., MacMeekin, W., Meekin, W., Wright, C., Perry, R. H., Kelly, P., Pearson, A. D., and Lunec, J. (1998) Expression of the ErbB-neuregulin signaling network during human cerebellar development: implications for the biology of medulloblastoma. Cancer Res. 58, 3932-3941
19. Gilbertson, R., Hernan, R., Pietsch, T., Pinto, L., Scotting, P., Allibone, R., Ellison, D., Perry, R., Pearson, A., and Lunec, J. (2001) Novel ERBB4 juxtamembrane splice variants are frequently expressed in childhood medulloblastoma. Genes Chromosomes Cancer 31, 288-294
20. Gilbertson, R. J., Bentley, L., Hernan, R., Junttila, T. T., Frank, A. J., Haapasalo, H., Connelly, M., Wetmore, C., Curran, T., Elenius, K., and Ellison, D. W. (2002) ERBB receptor signaling promotes ependymoma cell proliferation and represents a potential novel therapeutic target for this disease. Clin. Cancer Res. 8, 3054-3064
21. Klapper, L. N., Kirschbaum, M. H., Sela, M., and Yarden, Y. (2000) Biochemical and clinical implications of the ErbB/HER signaling network of growth factor receptors. Adv. Cancer Res. 77, 25-79
22. Starr, A., Greif, J., Vexler, A., Ashkenazy-Voghera, M., Gladesh, V., Rubin, C., Kerber, G., Marmor, S., Lev-Ari, S., Inbar, M., Yarden, Y., and Ben-Yosef, R. (2006) ErbB4 increases the proliferation potential of human lung cancer cells and its blockage can be used as a target for anti-cancer therapy. Int. J. Cancer 119, 269-274
23. Paatero, I., and Elenius, K. (2008) ErbB4 and its isoforms: patentable drug targets Recent Pat. DNA Gene Seq. 2, 27-33
24. Kang, S. M., and Lee, H. J. (2014) MicroRNAs in human lung cancer. Exp. Biol. Med. 239, 1505-1513
25. Guz, M., Rivero-Müller, A., Okon, E., Stenzel-Bembenek, A., Polberg, K., Somka, M., and Stepulak, A. (2014) MicroRNAs: role in lung cancer. Dis. Markers 2014, 218169
26. Calin, G. A., and Croce, C. M. (2006) MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857-866
27. Ma, L., and Weinberg, R. A. (2008) Micromanagers of malignancy: role of microRNAs in regulating metastasis. Trends Genet. 24, 448-456
28. Nicoloso, M. S., Spizzo, R., Shimizu, M., Rossi, S., and Calin, G. A. (2009) MicroRNAs: the micro steering wheel of tumour metastases. Nat. Rev. Cancer 9, 293-302
29. Heller, G., Weinzierl, M., Noll, C., Babinsky, V., Ziegler, B., Altenberger, C., Minichsdorfer, C., Lang, G., Döme, B., End-Pfützenreuter, A., Arns, B. M., Grin, Y., Klepetko, W., Zielinski, C. C., and Zöchbauer-Müller, S. (2012) Genome-wide miRNA expression profiling identifies miR-9-3 and miR-193a as targets for DNA methylation in non-small cell lung cancers. Clin. Cancer Res. 18, 1619-1629
30. Walter, B. A., Valera, V. A., Pinto, P. A., and Merino, M. J. (2013) Comprehensive microRNA profiling of prostate cancer. J. Cancer 4, 350-357
31. Tahiri, A., Leivonen, S. K., L-uders, T., Steinfeld, I., Ragle Aure, M., Geisler, J., Mäkelä, R., Nord, S., Riis, M. L. H., Yakhini, Z., Kleivi Sahlberg, K., Borresen-Dale, A. L., Perälä, M., Bukholm, I. R. K., and Kristensen, V. N. (2014) Deregulation of cancer-related miRNAs is a common event in both benign and malignant human breast tumors. Carcinogenesis 35, 76-85
32. Chen, D., Cabay, R. J., Jin, Y., Wang, A., Lu, Y., Shah-Khan, M., and Zhou, X. (2013) MicroRNA deregulations in head and neck squamous cell carcinomas. J. Oral Maxillofac. Res. 4, e2
33. Yong, F. L., Law, C. W., and Wang, C. W. (2013) Potentiality of a triple microRNA classifier: miR-193a-3p, miR-23a and miR-338-5p for early detection of colorectal cancer. BMC Cancer 13, 280
34. Gao, X. N., Lin, J., Li, Y. H., Gao, L., Wang, X. R., Wang, W., Kang, H. Y., Yan, G. T., Wang, L. L., and Yu, L. (2011) MicroRNA-193a represses c-kit expression and functions as a methylation-silenced tumor suppressor in acute myeloid leukemia. Oncogene 30, 3416-3428
35. Watson, J. A., Bryan, K., Williams, R., Popov, S., Vujanic, G., Coulomb, A., Boccon-Gibod, L., Graf, N., Pritchard-Jones, K., and O'Sullivan, M. (2013) miRNA profiles as a predictor of chemoresponsiveness in Wilms' tumor blastema. PLoS One 8, e53417
36. Iliopoulos, D., Rotem, A., and Struhl, K. (2011) Inhibition of miR-193a expression by Max and RXR- activates K-Ras and PLAU to mediate distinct aspects of cellular transformation. Cancer Res. 71, 5144-5153
37. Noh, H., Hong, S., Dong, Z., Pan, Z. K., Jing, Q., and Huang, S. (2011) Impaired microRNA processing facilitates breast cancer cell invasion by upregulating urokinase-type plasminogen activator expression. Genes Cancer 2, 140-150
38. Uhlmann, S., Mannsperger, H., Zhang, J. D., Horvat, E. A., Schmidt, C., Küblbeck, M., Henjes, F., Ward, A., Tschulena, U., Zweig, K., Korf, U., Wiemann, S., and Sahin, O. (2012) Global microRNA level regulation of EGFR-driven cell-cycle protein network in breast cancer. Mol. Syst. Biol. 8, 570
39. Nakano, H., Yamada, Y., Miyazawa, T., and Yoshida, T. (2013) Gain-offunction microRNA screens identify miR-193a regulating proliferation and apoptosis in epithelial ovarian cancer cells. Int. J. Oncol. 42, 1875-1882
40. Salvi, A., Conde, I., Abeni, E., Arici, B., Grossi, I., Specchia, C., Portolani, N., Barlati, S., and De Petro, G. (2013) Effects of miR-193a and sorafenib on hepatocellular carcinoma cells. Mol. Cancer 12, 162
41. Wang, J., Yang, B., Han, L., Li, X., Tao, H., Zhang, S., and Hu, Y. (2013) Demethylation of miR-9-3 and miR-193a genes suppresses proliferation and promotes apoptosis in non-small cell lung cancer cell lines. Cell Physiol. Biochem. 32, 1707-1719
42. Chen, X., Guo, X., Zhang, H., Xiang, Y., Chen, J., Yin, Y., Cai, X., Wang, K., Wang, G., Ba, Y., Zhu, L., Wang, J., Yang, R., Zhang, Y., Ren, Z., Zen, K., Zhang, J., and Zhang, C. Y. (2009) Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene 28, 1385-1392
43. Li, B., Blanc, J. M., Sun, Y., Yang, L., Zaorsky, N. G., Giacalone, N. J., Torossian, A., and Lu, B. (2014) Assessment of M867, a selective caspase-3 inhibitor, in an orthotopic mouse model for non-small cell lung carcinoma. Am. J. Cancer Res. 4, 161-171
44. Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P., and Burge, C. B. (2003) Prediction of mammalian microRNA targets. Cell 115, 787-798
45. John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C., and Marks, D. S. (2004) Human MicroRNA targets. PLoS Biol. 2, e363
46. Krek, A., Grün, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M., and Rajewsky, N. (2005) Combinatorial microRNA target predictions. Nat. Genet. 37, 495-500
47. Wang, X. C., Tian, L. L., Wu, H. L., Jiang, X. Y., Du, L. Q., Zhang, H., Wang, Y. Y., Wu, H. Y., Li, D. G., She, Y., Liu, Q. F., Fan, F. Y., and Meng, A. M. (2010) Expression of miRNA-130a in nonsmall cell lung cancer. Am. J. Med. Sci. 340, 385-388
48. Du, L., Schageman, J. J., Irnov, Girard, L., Hammond, S. M., Minna, J. D., Gazdar, A. F., and Pertsemlidis, A. (2010) MicroRNA expression distinguishes SCLC from NSCLC lung tumor cells and suggests a possible pathological relationship between SCLCs and NSCLCs. J. Exp. Clin. Cancer Res. 29, 75
49. Ambros, V. (2004) The functions of animal microRNAs. Nature 431, 350-355
50. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
51. He, L., and Hannon, G. J. (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522-531
52. Yu, T., Li, J., Yan, M., Liu, L., Lin, H., Zhao, F., Sun, L., Zhang, Y., Cui, Y., Zhang, F., He, X., and Yao, M. (2014) MicroRNA-193a-3p and-5p suppress the metastasis of human non-small-cell lung cancer by downregulating the ERBB4/PIK3R3/mTOR/S6K2 signaling pathway. Oncogene, in press
53. Esquela-Kerscher, A., and Slack, F. J. (2006) Oncomirs: microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259-269
54. Kwon, J. E., Kim, B. Y., Kwak, S. Y., Bae, I. H., and Han, Y. H. (2013) Ionizing radiation-inducible microRNA miR-193a-3p induces apoptosis by directly targeting Mcl-1. Apoptosis 18, 896-909
55. Ma, K., He, Y., Zhang, H., Fei, Q., Niu, D., Wang, D., Ding, X., Xu, H., Chen, X., and Zhu, J. (2012) DNA methylation-regulated miR-193a-3p dictates resistance of hepatocellular carcinoma to 5-fluorouracil via repression of SRSF2 expression. J. Biol. Chem. 287, 5639-5649
56. Aurisicchio, L., Marra, E., Luberto, L., Carlomosti, F., De Vitis, C., Noto, A., Gunes, Z., Roscilli, G., Mesiti, G., Mancini, R., Alimandi, M., and Ciliberto, G. (2012) Novel anti-ErbB3 monoclonal antibodies show therapeutic efficacy in xenografted and spontaneous mouse tumors. J. Cell. Physiol. 227, 3381-3388