MicroRNA-24 regulates XIAP to reduce the apoptosis threshold in cancer cells

Oncogene

Volumn 32, Issue 19, 2013, Pages 2442-2451

  Xie, Y ^a   Tobin, L A ^a   Camps, J ^b   Wangsa, D ^b   Yang, J ^a   Rao, M ^a   Witasp, E ^a,c   Awad, K S ^d   Yoo, N ^a   Ried, T ^b   Kwong, K F ^a,b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c Swedish Chemicals Agency   (Sweden)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

cancer; microRNA; XIAP

Indexed keywords

CASPASE; LUCIFERASE; MESSENGER RNA; MICRORNA 24; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; X LINKED INHIBITOR OF APOPTOSIS;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; BIOINFORMATICS; CANCER CELL; CHROMOSOME LOSS; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; DOWN REGULATION; GENE LOCUS; HUMAN; HUMAN CELL; KARYOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SITE DIRECTED MUTAGENESIS;

3' UNTRANSLATED REGIONS; APOPTOSIS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DOWN-REGULATION; HELA CELLS; HUMANS; MICRORNAS; NEOPLASMS; TRANSFECTION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84877617507     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.258     Document Type: Article

References (59)

1. Mashima T, Tsuruo T. Defects of the apoptotic pathway as therapeutic target against cancer. Drug Resist Updat 2005; 8: 339-343.
2. Dean EJ, Ranson M, Blackhall F, Holt SV, Dive C. Novel therapeutic targets in lung cancer: inhibitor of apoptosis proteins from laboratory to clinic. Cancer Treat Rev 2007; 33: 203-212.
3. Wang H, Yu SW, Koh DW, Lew J, Coombs C, Bowers W et al. Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J Neurosci 2004; 24: 10963-10973.
4. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998; 17: 1675-1687.
5. Geering B, Gurzeler U, Federzoni E, Kaufmann T, Simon HU. A novel TNFR1-triggered apoptosis pathway mediated by class IA PI3Ks in neutrophils. Blood 117: 5953-5962.
6. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW et al. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001; 104: 791-800.
7. Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES et al. Structural basis of caspase-7 inhibition by XIAP. Cell 2001; 104: 769-780.
8. Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM et al. Mechanism of XIAP-mediated inhibition of caspase-9. Mol Cell 2003; 11: 519-527.
9. Sun C, Cai M, Gunasekera AH, Meadows RP, Wang H, Chen J et al. NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP. Nature 1999; 401: 818-822.
10. Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J et al. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001; 410: 112-116.
11. Deveraux QL, Reed JC. IAP family proteins-suppressors of apoptosis. Genes Dev 1999; 13: 239-252.
12. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391: 806-811.
13. Diakos C, Zhong S, Xiao Y, Zhou M, Vasconcelos GM, Krapf G et al. TEL-AML1 regulation of survivin and apoptosis via miRNA-494 and miRNA-320a. Blood 2010; 116: 4885-4893.
14. Alajez NM, Lenarduzzi M, Ito E, Hui AB, Shi W, Bruce J et al. mir-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway. Cancer Res 2011; 71: 2381-2391.
15. Saini S, Yamamura S, Majid S, Shahryari V, Hirata H, Tanaka Y et al. MicroRNA-708 induces apoptosis and suppresses tumorigenicity in renal cancer cells. Cancer Res 2011; 71: 6208-6219.
16. Saini S, Majid S, Yamamura S, Tabatabai L, Suh SO, Shahryari V et al. Regulatory role of mir-203 in prostate cancer progression and metastasis. Clin Cancer Res 2010; 17: 5287-5298.
17. Siegel C, Li J, Liu F, Benashski SE, McCullough LD. miR-23a regulation of X-linked inhibitor of apoptosis (XIAP) contributes to sex differences in the response to cerebral ischemia. Proc Natl Acad Sci USA 2011; 108: 11662-11667.
18. Zhu W, Xu H, Zhu D, Zhi H, Wang T, Wang J et al. miR-200bc/429 cluster modulates multidrug resistance of human cancer cell lines by targeting BCL2 and XIAP. Cancer Chemother Pharmacol 2012; 69: 723-731.
19. Mishra PJ, Humeniuk R, Mishra PJ, Longo-Sorbello GSA, Banerjee D, Bertino JR. A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci USA 2007; 104: 13513-13518.
20. Wang Q, Huang Z, Xue HL, Jin CC, Ju XL, Han JDJ et al. MicroRNA miR-24 inhibits erythropoiesis by targeting activin type I receptor ALK4. Blood 2008; 111: 588-595.
21. Lal A, Kim HH, Abdelmohsen K, Kuwano Y, Pullmann R, Srikantan S et al. p16(INK4a) translation suppressed by miR-24. Plos One 2008; 3: e1864.
22. Lal A, Pan YF, Navarro F, Dykxhoorn DM, Moreau L, Meire E et al. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat Struct Mol Biol 2009; 16: 492-498.
23. 0 UTR microRNA recognition elements. Mol Cell 2009; 35: 610-625.
24. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294: 853-858.
25. Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L et al. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev 2002; 16: 720-728.
26. Tonon G, Gehlhaus KS, Yonescu R, Kaye FJ, Kirsch IR. Multiple reciprocal translocations in salivary gland mucoepidermoid carcinomas. Cancer Genet Cytogenet 2004; 152: 15-22.
27. Macville M, Schrock E, Padilla-Nash H, Keck C, Ghadimi BM, Zimonjic D et al. Comprehensive and definitive molecular cytogenetic characterization of HeLa cells by spectral karyotyping. Cancer Res 1999; 59: 141-150.
28. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23: 4051-4060.
29. Bao L, Dunham K, Lucas K. MAGE-A1, MAGE-A3, and NY-ESO-1 can be upregulated on neuroblastoma cells to facilitate cytotoxic T lymphocyte-mediated tumor cell killing. Cancer Immunol Immunother 2011; 60: 1299-1307.
30. Adair SJ, Hogan KT. Treatment of ovarian cancer cell lines with 5-aza-2'-deox-ycytidine upregulates the expression of cancer-testis antigens and class I major histocompatibility complex-encoded molecules. Cancer Immunol Immunother 2009; 58: 589-601.
31. Ulybina YM, Kuligina ES, Mitiushkina NV, Sherina NY, Baholdin DV, Voskresenskiy DA et al. Distribution of coding apoptotic gene polymorphisms in women with extreme phenotypes of breast cancer predisposition and tolerance. Tumori 2011; 97: 248-251.
32. Kang HG, Lee SJ, Chae MH, Lee WK, Cha SI, Kim CH et al. Identification of polymorphisms in the XIAP gene and analysis of association with lung cancer risk in a Korean population. Cancer Genet Cytogenet 2008; 180: 6-13.
33. Holcik M. Translational upregulation of the X-linked inhibitor of apoptosis. Ann N Y Acad Sci 2003; 1010: 249-258.
34. 0 UTRs regulate XIAP expression under normal growth conditions and during cellular stress. Nucleic Acids Res 2010; 38: 4665-4674.
35. Ku G, McManus MT. Behind the scenes of a small RNA gene-silencing pathway. Hum Gene Ther 2008; 19: 17-26.
36. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E et al. Inhibition of translational initiation by Let-7 microRNA in human cells. Science 2005; 309: 1573-1576.
37. Humphreys DT, Westman BJ, Martin DIK, Preiss T. MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc Natl Acad Sci USA 2005; 102: 16961-16966.
38. Wang BB, Love TM, Call ME, Doench JG, Novina CD. Recapitulation of short RNA-directed translational gene silencing in vitro. Mol Cell 2006; 22: 553-560.
39. Petersen CP, Bordeleau ME, Pelletier J, Sharp PA. Short RNAs repress translation after initiation in mammalian cells. Mol Cell 2006; 21: 533-542.
40. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K et al. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006; 312: 75-79.
41. 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: 13944-13949.
42. Liu L, Chen L, Xu Y, Li R, Du X. MicroRNA-195 promotes apoptosis and suppresses tumorigenicity of human colorectal cancer cells. Biochem Biophys Res Commun 2010; 400: 236-240.
43. Wang X, Liu P, Zhu H, Xu Y, Ma C, Dai X et al. miR-34a, a microRNA up-regulated in a double transgenic mouse model of Alzheimer's disease, inhibits bcl2 translation. Brain Res Bull 2009; 80: 268-273.
44. Zhu W, Shan X, Wang T, Shu Y, Liu P. miR-181b modulates multidrug resistance by targeting BCL2 in human cancer cell lines. Int J Cancer 2010; 127: 2520-2529.
45. Chhabra R, Adlakha YK, Hariharan M, Scaria V, Saini N. Upregulation of miR-23a-27a-24-2 cluster induces caspase-dependent and-independent apoptosis in human embryonic kidney cells. PLoS One 2009; 4: e5848.
46. Yoon S, Choi YC, Lee S, Jeong Y, Yoon J, Baek K. Induction of growth arrest by miR-542-3p that targets survivin. FEBS Lett 2010; 584: 4048-4052.
47. Eckelman BP, Salvesen GS, Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 2006; 7: 988-994.
48. Niederer F, Trenkmann M, Ospelt C, Karouzakis E, Neidhart M, Stanczyk J et al. Downregulation of microRNA-34a* in rheumatoid arthritis synovial fibroblasts promotes apoptosis resistance. Arthritis Rheum 2012; 64: 1771-1779.
49. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008; 455: 58-63.
50. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455: 64-71.
51. Qin W, Shi Y, Zhao B, Yao C, Jin L, Ma J et al. miR-24 regulates apoptosis by targeting the open reading frame (ORF) region of FAF1 in cancer cells. Plos One 2010; 5: e9429.
52. Walker JC, Harland RM. MicroRNA-24a is required to repress apoptosis in the developing neural retina. Genes Dev 2009; 23: 1046-1051.
53. Medina PP, Slack FJ. MicroRNAs and cancer: an overview. Cell Cycle 2008; 7: 2485-2492.
54. Agirre X, Vilas-Zornoza A, Jimenez-Velasco A, Martin-Subero JI, Cordeu L, Garate L et al. Epigenetic silencing of the tumor suppressor microRNA Hsa-miR-124a regulates CDK6 expression and confers a poor prognosis in acute lymphoblastic leukemia. Cancer Res 2009; 69: 4443-4453.
55. Maragkakis M, Reczko M, Simossis VA, Alexiou P, Papadopoulos GL, Dalamagas T et al. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucleic Acids Res 2009(Web Server issue): W273-W276.
56. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007; 27: 91-105.
57. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS Biol. 2004; 2: e363.
58. Kruger J, Rehmsmeier M. RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 2006; 34(Web Server issue): W451-W454.
59. Padilla-Nash HM, Barenboim-Stapleton L, Difilippantonio MJ, Ried T. Spectral kar-yotyping analysis of human and mouse chromosomes. Nat Protoc 2006; 1: 3129-3142.