Mir-660 is downregulated in lung cancer patients and its replacement inhibits lung tumorigenesis by targeting MDM2-p53 interaction

Cell Death and Disease

Volumn 5, Issue 12, 2014, Pages

  Fortunato, O ^a   Boeri, M ^a   Moro, M ^a   Verri, C ^a   Mensah, M ^a   Conte, D ^a   Caleca, L ^a   Roz, L ^a   Pastorino, U ^a   Sozzi, G ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

LENTIVIRUS VECTOR; MESSENGER RNA; MICRORNA; MICRORNA 660; PROTEIN; PROTEIN MDM2; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; MIRN-660 MICRORNA, MOUSE; MIRN660 MICRORNA, HUMAN; PROTEIN BINDING;

A549 CELL LINE; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CANCER TISSUE; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; FEMALE; GENE LOCUS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LT43 CELL LINE; LUNG CANCER; LUNG CANCER CELL LINE; LUNG CARCINOGENESIS; MIGRATION INHIBITION; MITOSIS INHIBITION; MOLECULARLY TARGETED THERAPY; MOUSE; NCI H460 CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STABLE EXPRESSION; TUMOR XENOGRAFT; WILD TYPE; ANIMAL; CARCINOGENESIS; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; SCID MOUSE;

MUS;

AGED; ANIMALS; APOPTOSIS; CARCINOGENESIS; CELL PROLIFERATION; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MALE; MICE; MICE, SCID; MICRORNAS; MIDDLE AGED; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84926618053     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.507     Document Type: Article

References (63)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Ettinger DS, Akerley W, Bepler G, Blum MG, Chang A, Cheney RT et al. Non-small cell lung cancer. J Natl Compr Canc Netw 2010; 8: 740-801.
3. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004; 350: 2129-2139.
4. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007; 448: 561-566.
5. Youlden DR, Cramb SM, Baade PD. The International Epidemiology of Lung Cancer: geographical distribution and secular trends. J Thorac Oncol 2008; 3: 819-831.
6. Jackman DM, Johnson BE. Small-cell lung cancer. Lancet 2005; 366: 1385-1396.
7. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med 2008; 359: 1367-1380.
8. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-297.
9. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
10. 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: 15-20.
11. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294: 853-858.
12. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 2008; 9: 405-414.
13. He L, He X, Lim LP, de SE, Xuan Z, Liang Y et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447: 1130-1134.
14. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A 2005; 102: 13944-13949.
15. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007; 449: 682-688.
16. Raponi M, Dossey L, Jatkoe T, Wu X, Chen G, Fan H et al. MicroRNA classifiers for predicting prognosis of squamous cell lung cancer. Cancer Res 2009; 69: 5776-5783.
17. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006; 9: 189-198.
18. 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: 3753-3756.
19. Bishop JA, Benjamin H, Cholakh H, Chajut A, Clark DP, Westra WH. Accurate classification of non-small cell lung carcinoma using a novel microRNA-based approach. Clin Cancer Res 2010; 16: 610-619.
20. Boeri M, Verri C, Conte D, Roz L, Modena P, Facchinetti F et al. MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer. Proc Natl Acad Sci U S A 2011; 108: 3713-3718.
21. Sozzi G, Boeri M, Rossi M, Verri C, Suatoni P, Bravi F et al. Clinical Utility of a Plasma-Based miRNA Signature Classifier Within Computed Tomography Lung Cancer Screening: A Correlative MILD Trial Study. J Clin Oncol 2014; 32: 768-773.
22. Zhu DX, Zhu W, Fang C, Fan L, Zou ZJ, Wang YH et al. miR-181a/b significantly enhances drug sensitivity in chronic lymphocytic leukemia cells via targeting multiple anti-apoptosis genes. Carcinogenesis 2012; 33: 1294-1301.
23. Ferrer G, Navarro A, Hodgson K, Aymerich M, Pereira A, Baumann T et al. MicroRNA expression in chronic lymphocytic leukemia developing autoimmune hemolytic anemia. Leuk Lymphoma 2013; 54: 2016-2022.
24. Pizzimenti S, Ferracin M, Sabbioni S, Toaldo C, Pettazzoni P, Dianzani MU et al. MicroRNA expression changes during human leukemic HL-60 cell differentiation induced by 4-hydroxynonenal, a product of lipid peroxidation. Free Radic Biol Med 2009; 46: 282-288.
25. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323-331.
26. Wu L, Levine AJ. Differential regulation of the p21/WAF-1 and mdm2 genes after high-dose UV irradiation: p53-dependent and p53-independent regulation of the mdm2 gene. Mol Med 1997; 3: 441-451.
27. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997; 420: 25-27.
28. Montes de Oca LR, Wagner DS, Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 1995; 378: 203-206.
29. Chen J, Wu X, Lin J, Levine AJ. mdm-2 inhibits the G1 arrest and apoptosis functions of the p53 tumor suppressor protein. Mol Cell Biol 1996; 16: 2445-2452.
30. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997; 387: 299-303.
31. Moll UM, Petrenko O. The MDM2-p53 interaction. Mol Cancer Res 2003; 1: 1001-1008.
32. Kussie PH, Gorina S, Marechal V, Elenbaas B, Moreau J, Levine AJ et al. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 1996; 274: 948-953.
33. Momand J, Zambetti GP, Olson DC, George D, Levine AJ. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992; 69: 1237-1245.
34. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997; 387: 296-299.
35. Lai Z, Ferry KV, Diamond MA, Wee KE, Kim YB, Ma J et al. Human mdm2 mediates multiple mono-ubiquitination of p53 by a mechanism requiring enzyme isomerization. J Biol Chem 2001; 276: 31357-31367.
36. Feng J, Tamaskovic R, Yang Z, Brazil DP, Merlo A, Hess D et al. Stabilization of Mdm2 via decreased ubiquitination is mediated by protein kinase B/Akt-dependent phosphorylation. J Biol Chem 2004; 279: 35510-35517.
37. Oliner JD, Kinzler KW, Meltzer PS, George DL, Vogelstein B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 1992; 358: 80-83.
38. Capoulade C, Bressac-de Paillerets B, Lefrere I, Ronsin M, Feunteun J, Tursz T et al. Overexpression of MDM2, due to enhanced translation, results in inactivation of wild-type p53 in Burkitt's lymphoma cells. Oncogene 1998; 16: 1603-1610.
39. Marchetti A, Buttitta F, Girlando S, Dalla PP, Pellegrini S, Fina P et al. mdm2 gene alterations and mdm2 protein expression in breast carcinomas. J Pathol 1995; 175: 31-38.
40. Marchetti A, Buttitta F, Pellegrini S, Merlo G, Chella A, Angeletti CA et al. mdm2 gene amplification and overexpression in non-small cell lung carcinomas with accumulation of the p53 protein in the absence of p53 gene mutations. Diagn Mol Pathol 1995; 4: 93-97.
41. Riou G, Barrois M, Prost S, Terrier MJ, Theodore C, Levine AJ. The p53 and mdm-2 genes in human testicular germ-cell tumors. Mol Carcinog 1995; 12: 124-131.
42. Zhang J, Sun Q, Zhang Z, Ge S, Han ZG, Chen WT. Loss of microRNA-143/145 disturbs cellular growth and apoptosis of human epithelial cancers by impairing the MDM2-p53 feedback loop. Oncogene 2013; 32: 61-69.
43. Suh SS, Yoo JY, Nuovo GJ, Jeon YJ, Kim S, Lee TJ et al. MicroRNAs/TP53 feedback circuitry in glioblastoma multiforme. Proc Natl Acad Sci U S A 2012; 109: 5316-5321.
44. Pastorino U, Bellomi M, Landoni C, De Fiori E, Arnaldi P, Picchio M et al. Early lung-cancer detection with spiral CTand positron emission tomography in heavy smokers: 2-year results. Lancet 2003; 362: 593-597.
45. Pastorino U, Rossi M, Rosato V, Marchiano A, Sverzellati N, Morosi C et al. Annual or biennial CT screening versus observation in heavy smokers: 5-year results of the MILD trial. Eur J Cancer Prev 2012; 21: 308-315.
46. Sozzi G, Pastorino U, Croce CM. MicroRNAs and lung cancer: from markers to targets. Cell Cycle 2011; 10: 2045-2046.
47. Peng Y, Dai Y, Hitchcock C, Yang X, Kassis ES, Liu L et al. Insulin growth factor signaling is regulated by microRNA-486, an underexpressed microRNA in lung cancer. Proc Natl Acad Sci U S A 2013; 110: 15043-15048.
48. Du L, Schageman JJ, Subauste MC, Saber B, Hammond SM, Prudkin L et al. miR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Mol Cancer Res 2009; 7: 1234-1243.
49. Trang P, Weidhaas JB, Slack FJ. MicroRNAs as potential cancer therapeutics. Oncogene 2008; 27: S52-S57.
50. Leonard CJ, Canman CE, Kastan MB. The role of p53 in cell-cycle control and apoptosis: implications for cancer. Important Adv Oncol 1995: 33-42.
51. Roger L, Gadea G, Roux P. Control of cell migration: a tumour suppressor function for p53? Biol Cell 2006; 98: 141-152.
52. Vousden KH. p53: death star. Cell 2000; 103: 691-694.
53. Gadea G, Roger L, Anguille C, de Toledo M, Gire V, Roux P. TNFalpha induces sequential activation of Cdc42-and p38/p53-dependent pathways that antagonistically regulate filopodia formation. J Cell Sci 2004; 117: 6355-6364.
54. Yokota J, Kohno T. Molecular footprints of human lung cancer progression. Cancer Sci 2004; 95: 197-204.
55. Clinical Lung Cancer Genome Project (CLCGP)Network Genomic Medicine (NGM), A genomics-based classification of human lung tumors. Sci Transl Med 2013; 5: 209ra153.
56. Freedman DA, Wu L, Levine AJ. Functions of the MDM2 oncoprotein. Cell Mol Life Sci 1999; 55: 96-107.
57. Higashiyama M, Doi O, Kodama K, Yokouchi H, Kasugai T, Ishiguro S et al. MDM2 gene amplification and expression in non-small-cell lung cancer: immunohistochemical expression of its protein is a favourable prognostic marker in patients without p53 protein accumulation. Br J Cancer 1997; 75: 1302-1308.
58. Momand J, Jung D, Wilczynski S, Niland J. The MDM2 gene amplification database. Nucleic Acids Res 1998; 26: 3453-3459.
59. Tovar C, Rosinski J, Filipovic Z, Higgins B, Kolinsky K, Hilton H et al. Small-molecule MDM2 antagonists reveal aberrant p53 signaling in cancer: implications for therapy. Proc Natl Acad Sci USA 2006; 103: 1888-1893.
60. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004; 303: 844-848.
61. Allen JG, Bourbeau MP, Wohlhieter GE, Bartberger MD, Michelsen K, Hungate R et al. Discovery and optimization of chromenotriazolopyrimidines as potent inhibitors of the mouse double minute 2-tumor protein 53 protein-protein interaction. J Med Chem 2009; 52: 7044-7053.
62. Chene P. Inhibiting the p53-MDM2 interaction: an important target for cancer therapy. Nat Rev Cancer 2003; 3: 102-109.
63. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ et al. The remaining authors declare no conflict of interest. Guidelines for the welfare and use of animals in cancer research. Br J Cancer 2010; 102: 1555-1577.