Large-scale screening identifies a novel microRNA, miR-15a-3p, which induces apoptosis in human cancer cell lines

RNA Biology

Volumn 10, Issue 2, 2013, Pages 287-300

  Druz, Aliaksandr ^a,b   Chen, Yu Chi ^c   Guha, Rajarshi ^c   Betenbaugh, Michael ^b   Martin, Scott E ^c   Shiloach, Joseph ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b Johns Hopkins University   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Apoptosis; BCL XL; Cancer cells; Caspase; MicroRNA

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CASPASE 3; CASPASE 7; FIBROBLAST GROWTH FACTOR RECEPTOR 2; MICRORNA; MICRORNA 15A; MICRORNA 15A 3P; MICRORNA 16; PROTEIN BCL XL; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BCL2L1 GENE; BIOINFORMATICS; BREAST CANCER; CANCER CELL CULTURE; CELL STRAIN HEK293; CELL VIABILITY; COLORECTAL CARCINOMA; CONTROLLED STUDY; DRUG SCREENING; GENE CLUSTER; GENE EXPRESSION; GENETIC SCREENING; HELA CELL; HUMAN; HUMAN CELL; LUNG CANCER; MICROARRAY ANALYSIS; MOLECULAR LIBRARY; MOLECULARLY TARGETED THERAPY; MOUSE; MYBL2 GENE; NAIP5 GENE; NONHUMAN; PANCREAS CANCER; UTERINE CERVIX CANCER;

EID: 84874616942     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.23339     Document Type: Article

References (70)

1. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9:102-14; PMID:18197166; http://dx.doi. org/10.1038/nrg2290.
2. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99:15524-9; PMID:12434020; http://dx.doi. org/10.1073/pnas.242606799.
3. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 2006; 6:259-69; PMID:16557279; http://dx.doi.org/10.1038/nrc1840.
4. Jovanovic M, Hengartner MO. miRNAs and apoptosis: RNAs to die for. Oncogene 2006; 25:6176-87; PMID:17028597; http://dx.doi.org/10.1038/sj.onc. 1209912.
5. Lynam-Lennon N, Maher SG, Reynolds JV. The roles of microRNA in cancer and apoptosis. Biol Rev Camb Philos Soc 2009; 84:55-71; PMID:19046400; http://dx.doi.org/10.1111/j.1469-185X.2008.00061.x.
6. 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 USA 2005; 102:13944-9; PMID:16166262; http://dx.doi. org/10.1073/pnas.0506654102.
7. Druz A, Chu C, Majors B, Santuary R, Betenbaugh M, Shiloach J. A novel microRNA mmu-miR-466h affects apoptosis regulation in mammalian cells. Biotechnol Bioeng 2011; 108:1651-61; PMID:21337326; http://dx.doi.org/10.1002/ bit.23092.
8. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17:193-9; PMID:19461653; http://dx.doi.org/10.1038/cdd.2009.56.
9. Ovcharenko D, Kelnar K, Johnson C, Leng N, Brown D. Genome-scale microRNA and small interfering RNA screens identify small RNA modulators of TRAILinduced apoptosis pathway. Cancer Res 2007; 67:10782-8; PMID:18006822; http://dx.doi.org/10.1158/0008-5472.CAN-07-1484.
10. Shimizu S, Takehara T, Hikita H, Kodama T, Miyagi T, Hosui A, et al. The let-7 family of microRNAs inhibits Bcl-xL expression and potentiates sorafenib-induced apoptosis in human hepatocellular carcinoma. J Hepatol 2010; 52:698-704; PMID:20347499; http://dx.doi. org/10.1016/j.jhep.2009.12.024.
11. Caroppi P, Sinibaldi F, Fiorucci L, Santucci R. Apoptosis and human diseases: mitochondrion damage and lethal role of released cytochrome C as proapoptotic protein. Curr Med Chem 2009; 16:4058-65; PMID:19754424; http://dx.doi.org/10.2174/092986709789378206.
12. Fischer U, Schulze-Osthoff K. New approaches and therapeutics targeting apoptosis in disease. Pharmacol Rev 2005; 57:187-215; PMID:15914467; http://dx.doi. org/10.1124/pr.57.2.6.
13. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995; 267:1456-62; PMID:7878464; http://dx.doi.org/10.1126/science. 7878464.
14. Klener P Jr., Andera L, Klener P, Necas E, Zivný J. Cell death signalling pathways in the pathogenesis and therapy of haematologic malignancies: overview of apoptotic pathways. Folia Biol (Praha) 2006; 52:34-44; PMID:17007108.
15. Nicholson DW. From bench to clinic with apoptosis-based therapeutic agents. Nature 2000; 407:810-6; PMID:11048733; http://dx.doi. org/10.1038/35037747.
16. Krajewska M, Moss SF, Krajewski S, Song K, Holt PR, Reed JC. Elevated expression of Bcl-X and reduced Bak in primary colorectal adenocarcinomas. Cancer Res 1996; 56:2422-7; PMID:8625322.
17. Liu QY, Stein CA. Taxol and estramustine-induced modulation of human prostate cancer cell apoptosis via alteration in bcl-xL and bak expression. Clin Cancer Res 1997; 3:2039-46; PMID:9815595.
18. Sánchez-Beato M, Sánchez-Aguilera A, Piris MA. Cell cycle deregulation in B-cell lymphomas. Blood 2003; 101:1220-35; PMID:12393483; http://dx.doi. org/10.1182/blood-2002-07-2009.
19. Watanabe J, Kushihata F, Honda K, Sugita A, Tateishi N, Mominoki K, et al. Prognostic significance of Bcl-xL in human hepatocellular carcinoma. Surgery 2004; 135:604-12; PMID:15179366; http://dx.doi. org/10.1016/j.surg.2003.11.015.
20. Xu Z, Friess H, Solioz M, Aebi S, Korc M, Kleeff J, et al. Bcl-x(L) antisense oligonucleotides induce apoptosis and increase sensitivity of pancreatic cancer cells to gemcitabine. Int J Cancer 2001; 94:268-74; PMID:11668508; http://dx.doi.org/10.1002/ijc.1447.
21. Minn AJ, Rudin CM, Boise LH, Thompson CB. Expression of bcl-xL can confer a multidrug resistance phenotype. Blood 1995; 86:1903-10; PMID:7655019.
22. Schmitt E, Sané AT, Steyaert A, Cimoli G, Bertrand R. The Bcl-xL and Bax-alpha control points: modulation of apoptosis induced by cancer chemotherapy and relation to TPCK-sensitive protease and caspase activation. Biochem Cell Biol 1997; 75:301-14; PMID:9493953.
23. Chu F, Borthakur A, Sun X, Barkinge J, Gudi R, Hawkins S, et al. The Siva-1 putative amphipathic helical region (SAH) is sufficient to bind to BCL-XL and sensitize cells to UV radiation induced apoptosis. Apoptosis 2004; 9:83-95; PMID:14739602; http://dx.doi.org/10.1023/B:APPT.0000012125.01799.4c.
24. Pollman MJ, Hall JL, Mann MJ, Zhang L, Gibbons GH. Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease. Nat Med 1998; 4:222-7; PMID:9461197; http://dx.doi. org/10.1038/nm0298-222.
25. Chung N, Zhang XD, Kreamer A, Locco L, Kuan PF, Bartz S, et al. Median absolute deviation to improve hit selection for genome-scale RNAi screens. J Biomol Screen 2008; 13:149-58; PMID:18216396; http://dx.doi.org/10.1177/ 1087057107312035.
26. Tsuruta T, Kozaki K, Uesugi A, Furuta M, Hirasawa A, Imoto I, et al. miR-152 is a tumor suppressor microRNA that is silenced by DNA hypermethylation in endometrial cancer. Cancer Res 2011; 71:6450-62; PMID:21868754; http://dx.doi.org/10.1158/0008-5472.CAN-11-0364.
27. Uesugi A, Kozaki K, Tsuruta T, Furuta M, Morita K, Imoto I, et al. The tumor suppressive microRNA miR-218 targets the mTOR component Rictor and inhibits AKT phosphorylation in oral cancer. Cancer Res 2011; 71:5765-78; PMID:21795477; http://dx.doi. org/10.1158/0008-5472.CAN-11-0368.
28. Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002; 297:2056-60; PMID:12154197; http://dx.doi. org/10.1126/science.1073827.
29. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008; 36(Database issue):D149-53; PMID:18158296; http://dx.doi.org/10.1093/nar/gkm995.
30. Maragkakis M, Vergoulis T, Alexiou P, Reczko M, Plomaritou K, Gousis M, et al. DIANA-microT Web server upgrade supports Fly and Worm miRNA target prediction and bibliographic miRNA to disease association. Nucleic Acids Res 2011; 39(Web Server issue):W145-8; PMID:21551220; http://dx.doi. org/10.1093/nar/gkr294.
31. Grassilli E, Salomoni P, Perrotti D, Franceschi C, Calabretta B. Resistance to apoptosis in CTLL-2 cells overexpressing B-Myb is associated with B-Mybdependent bcl-2 induction. Cancer Res 1999; 59:2451-6; PMID:10344757.
32. Srinivasula SM, Ashwell JD. IAPs: what's in a name? Mol Cell 2008; 30:123-35; PMID:18439892; http://dx.doi. org/10.1016/j.molcel.2008.03.008.
33. Kim R. Unknotting the roles of Bcl-2 and Bcl-xL in cell death. Biochem Biophys Res Commun 2005; 333:336-43; PMID:15922292; http://dx.doi.org/10.1016/j. bbrc.2005.04.161.
34. Pardo OE, Wellbrock C, Khanzada UK, Aubert M, Arozarena I, Davidson S, et al. FGF-2 protects small cell lung cancer cells from apoptosis through a complex involving PKCepsilon, B-Raf and S6K2. EMBO J 2006; 25:3078-88; PMID:16810323; http://dx.doi. org/10.1038/sj.emboj.7601198.
35. Qiu H, Yashiro M, Zhang X, Miwa A, Hirakawa KA. A FGFR2 inhibitor, Ki23057, enhances the chemosensitivity of drug-resistant gastric cancer cells. Cancer Lett 2011; 307:47-52; PMID:21482024; http://dx.doi. org/10.1016/j.canlet. 2011.03.015.
36. Weston K. Myb proteins in life, death and differentiation. Curr Opin Genet Dev 1998; 8:76-81; PMID:9529609; http://dx.doi.org/10.1016/S0959-437X(98) 80065-8.
37. Hikita H, Takehara T, Shimizu S, Kodama T, Shigekawa M, Iwase K, et al. The Bcl-xL inhibitor, ABT-737, efficiently induces apoptosis and suppresses growth of hepatoma cells in combination with sorafenib. Hepatology 2010; 52:1310-21; PMID:20799354; http://dx.doi. org/10.1002/hep.23836.
38. Kostanová-Poliaková D, Sabová L. Anti-apoptotic proteins-targets for chemosensitization of tumor cells and cancer treatment. Neoplasma 2005; 52:441-9; PMID:16284687.
39. Wang ZX, Yang JS, Pan X, Wang JR, Li J, Yin YM, et al. Functional and biological analysis of Bcl-xL expression in human osteosarcoma. Bone 2010; 47:445-54; PMID:20580954; http://dx.doi.org/10.1016/j. bone.2010.05.027.
40. Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 2009; 10:141-8; PMID:19145236; http://dx.doi.org/10.1038/nrm2619.
41. Kuhn DE, Martin MM, Feldman DS, Terry AV Jr., Nuovo GJ, Elton TS. Experimental validation of miRNA targets. Methods 2008; 44:47-54; PMID:18158132; http://dx.doi.org/10.1016/j.ymeth.2007.09.005.
42. Xiao F, Zuo Z, Cai G, Kang S, Gao X, Li T. miRecords: an integrated resource for microRNA-target interactions. Nucleic Acids Res 2009; 37(Database issue):D105-10; PMID:18996891; http://dx.doi.org/10.1093/nar/gkn851.
43. Cheng AM, Byrom MW, Shelton J, Ford LP. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 2005; 33:1290-7; PMID:15741182; http://dx.doi.org/10.1093/ nar/gki200.
44. Liu J, Zheng M, Tang YL, Liang XH, Yang Q. MicroRNAs, an active and versatile group in cancers. Int J Oral Sci 2011; 3:165-75; PMID:22010574; http://dx.doi.org/10.4248/IJOS11063.
45. Matsubara H, Takeuchi T, Nishikawa E, Yanagisawa K, Hayashita Y, Ebi H, et al. Apoptosis induction by antisense oligonucleotides against miR-17-5p and miR-20a in lung cancers overexpressing miR-17-92. Oncogene 2007; 26:6099-105; PMID:17384677; http://dx.doi. org/10.1038/sj.onc.1210425.
46. Porkka KP, Pfeiffer MJ, Waltering KK, Vessella RL, Tammela TL, Visakorpi T. MicroRNA expression profiling in prostate cancer. Cancer Res 2007; 67:6130-5; PMID:17616669; http://dx.doi.org/10.1158/0008-5472.CAN-07-0533.
47. Garofalo M, Quintavalle C, Di Leva G, Zanca C, Romano G, Taccioli C, et al. MicroRNA signatures of TRAIL resistance in human non-small cell lung cancer. Oncogene 2008; 27:3845-55; PMID:18246122; http://dx.doi.org/10.1038/onc.2008.6.
48. Mott JL, Kobayashi S, Bronk SF, Gores GJ. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 2007; 26:6133-40; PMID:17404574; http://dx.doi. org/10.1038/sj.onc.1210436.
49. Hsu CK, Rishi AK, Li XS, Dawson MI, Reichert U, Shroot B, et al. Bcl-X(L) expression and its downregulation by a novel retinoid in breast carcinoma cells. Exp Cell Res 1997; 232:17-24; PMID:9141616; http://dx.doi.org/10.1006/ excr.1997.3509.
50. Barisi K, Petrik J, Rumora L. Biochemistry of apoptotic cell death. Acta Pharm 2003; 53:151-64; PMID:14769239.
51. Finucane DM, Bossy-Wetzel E, Waterhouse NJ, Cotter TG, Green DR. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J Biol Chem 1999; 274:2225-33; PMID:9890985; http://dx.doi.org/10.1074/jbc.274.4.2225.
52. Majors BS, Betenbaugh MJ, Chiang GG. Links between metabolism and apoptosis in mammalian cells: applications for anti-apoptosis engineering. Metab Eng 2007; 9:317-26; PMID:17611135; http://dx.doi. org/10.1016/j.ymben.2007.05. 003.
53. Lam M, Bhat MB, Nuñez G, Ma J, Distelhorst CW. Regulation of Bcl-xl channel activity by calcium. J Biol Chem 1998; 273:17307-10; PMID:9651311; http://dx.doi.org/10.1074/jbc.273.28.17307.
54. Benito A, Silva M, Grillot D, Nuñez G, Fernández-Luna JL. Apoptosis induced by erythroid differentiation of human leukemia cell lines is inhibited by Bcl-XL. Blood 1996; 87:3837-43; PMID:8611710.
55. Dole MG, Jasty R, Cooper MJ, Thompson CB, Nuñez G, Castle VP. Bcl-xL is expressed in neuroblastoma cells and modulates chemotherapy-induced apoptosis. Cancer Res 1995; 55:2576-82; PMID:7780971.
56. Kondo S, Shinomura Y, Kanayama S, Higashimoto Y, Miyagawa JI, Minami T, et al. Over-expression of bcl-xL gene in human gastric adenomas and carcinomas. Int J Cancer 1996; 68:727-30; PMID:8980174; http://dx.doi.org/10.1002/(SICI) 1097-0215(19961211)68:6>727::AID-IJC6<3.0.CO;2-5.
57. Liu JR, Fletcher B, Page C, Hu C, Nunez G, Baker V. Bcl-xL is expressed in ovarian carcinoma and modulates chemotherapy-induced apoptosis. Gynecol Oncol 1998; 70:398-403; PMID:9790794; http://dx.doi. org/10.1006/gyno.1998.5125.
58. Kondo S, Shinomura Y, Kanayama S, Higashimoto Y, Kiyohara T, Zushi S, et al. Modulation of apoptosis by endogenous Bcl-xL expression in MKN-45 human gastric cancer cells. Oncogene 1998; 17:2585-91; PMID:9840921; http://dx.doi.org/10.1038/sj.onc.1202194.
59. Lee SK, Calin GA. Non-coding RNAs and cancer: new paradigms in oncology. Discov Med 2011; 11:245-54; PMID:21447283.
60. Kasinski AL, Slack FJ. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer 2011; 11:849-64; PMID:22113163; http://dx.doi.org/10.1038/ nrc3166.
61. Bandi N, Vassella E. miR-34a and miR-15a/16 are co-regulated in non-small cell lung cancer and control cell cycle progression in a synergistic and Rb-dependent manner. Mol Cancer 2011; 10:55; PMID:21575235; http://dx.doi.org/ 10.1186/1476-4598-10-55.
62. Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, et al. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 2008; 14:1271-7; PMID:18931683; http://dx.doi.org/10.1038/nm.1880.
63. Gao SM, Xing CY, Chen CQ, Lin SS, Dong PH, Yu FJ. miR-15a and miR-16-1 inhibit the proliferation of leukemic cells by down-regulating WT1 protein level. J Exp Clin Cancer Res 2011; 30:110; PMID:22133358; http://dx.doi.org/10. 1186/1756-9966-30-110.
64. Druz A, Betenbaugh M, Shiloach J. Glucose depletion activates mmu-miR-466h-5p expression through oxidative stress and inhibition of histone deacetylation. Nucleic Acids Res 2012; 40:7291-302; PMID:22638581; http://dx.doi.org/10.1093/nar/gks452.
65. Mishra PK, Gorantla VR, Akhtar N, Tamrakar P, Jain SK, Maudar KK. Analysis of cellular response to isocyanate using N-succinimidyl N-methylcarbamate exposure in cultured mammalian cells. Environ Mol Mutagen 2009; 50:328-36; PMID:19197993; http://dx.doi.org/10.1002/em.20469.
66. Mishra PK, Raghuram GV, Bhargava A, Ahirwar A, Samarth R, Upadhyaya R, et al. In vitro and in vivo evaluation of the anticarcinogenic and cancer chemopreventive potential of a flavonoid-rich fraction from a traditional Indian herb Selaginella bryopteris. Br J Nutr 2011; 106:1154-68; PMID:21736819; http://dx.doi. org/10.1017/S0007114511001498.
67. Raghuram GV, Pathak N, Jain D, Panwar H, Pandey H, Jain SK, et al. Molecular mechanisms of isocyanate induced oncogenic transformation in ovarian epithelial cells. Reprod Toxicol 2010; 30:377-86; PMID:20685613; http://dx.doi.org/10.1016/j.reprotox. 2010.05.087.
68. Chiang GG, Sisk WP. Bcl-x(L) mediates increased production of humanized monoclonal antibodies in Chinese hamster ovary cells. Biotechnol Bioeng 2005; 91:779-92; PMID:15986489; http://dx.doi.org/10.1002/bit.20551.
69. Lee CY, Johnson RL, Wichterman-Kouznetsova J, Guha R, Ferrer M, Tuzmen P, et al. High-throughput screening for genes that prevent excess DNA replication in human cells and for molecules that inhibit them. Methods 2012; 57:234-48; PMID:22503772; http://dx.doi.org/10.1016/j.ymeth.2012.03.031.
70. Zhang XD. Illustration of SSMD, z score, SSMD, z score, and t statistic for hit selection in RNAi high-throughput screens. J Biomol Screen 2011; 16:775-85; PMID:21515799; http://dx.doi. org/10.1177/1087057111405851.