MicroRNAs in autophagy and their emerging roles in crosstalk with apoptosis

Autophagy

Volumn 8, Issue 6, 2012, Pages 873-882

  Xu, Jianzhen ^a   Wang, Yanfei ^b   Tan, Xiaorong ^a   Jing, Hongjuan ^a  

^a HENAN UNIVERSITY OF TECHNOLOGY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Apoptosis; Autophagy; Cancers; Cell signaling; MiRNAs

Indexed keywords

BECLIN 1; BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; CASPASE 8; HISTONE DEACETYLASE; MICRORNA; MICRORNA 101; MICRORNA 17; MICRORNA 196; MICRORNA 204; MICRORNA 206; MICRORNA 30A; MICRORNA 9; ONCOPROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; APOPTOSIS; AUTOPHAGY; BREAST CANCER; CANCER GROWTH; CELL FATE; CROHN DISEASE; DISEASE COURSE; HUMAN; NONHUMAN; PROTEIN EXPRESSION; REVIEW; RNA BINDING; RNA PROCESSING;

EID: 84864872512     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.19629     Document Type: Review

References (100)

1. Levine B, Kroemer G.. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
2. Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 2008; 9:1004-10; PMID:18971948; http://dx.doi.org/10.1038/ nrm2529
3. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136:215-33; PMID:19167326; http://dx.doi.org/10.1016/j.cell.2009.01.002
4. Xu J, Wong C. A computational screen for mouse signaling pathways targeted by microRNA clusters. RNA 2008; 14:1276-83; PMID:18511500; http://dx.doi.org/10.1261/rna.997708
5. Megraw M, Sethupathy P, Corda B, Hatzigeorgiou AG. miRGen: a database for the study of animal microRNA genomic organization and function. Nucleic Acids Res 2007; 35(Database issue):D149-55; PMID:17108354; http://dx.doi.org/10.1093/ nar/gkl904
6. 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; 23:4051-60; PMID:15372072; http://dx.doi.org/10.1038/sj.emboj.7600385
7. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Mol Cell 2007; 28:328-36; PMID:17964270; http://dx.doi.org/10.1016/j. molcel.2007.09.028
8. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007; 130:89-100; PMID:17599402; http://dx.doi.org/10.1016/j.cell.2007.06.028
9. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature 2007; 448:83-6; PMID:17589500; http://dx.doi.org/10. 1038/nature05983
10. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008; 320:1185-90; PMID:18483398; http://dx.doi.org/10.1126/science.1159151
11. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010; 466:835-40; PMID:20703300; http://dx.doi.org/10.1038/nature09267
12. Li L, Xu J, Yang D, Tan X, Wang H. Computational approaches for microRNA studies: a review. Mamm Genome 2010; 21:1-12; PMID:20012966; http://dx.doi.org/10.1007/s00335-009-9241-2
13. Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009; 136:669-87; PMID:19239888; http://dx.doi.org/10.1016/j.cell.2009.01.046
14. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006; 103:2257-61; PMID:16461460; http://dx.doi.org/ 10.1073/pnas.0510565103
15. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, et al. 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; PMID:14973191; http://dx.doi.org/10.1073/pnas.0307323101
16. Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X, et al. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy 2009; 5:816-23; PMID:19535919
17. Mellios N, Huang HS, Grigorenko A, Rogaev E, Akbarian S. A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of BDNF in prefrontal cortex. Hum Mol Genet 2008; 17:3030-42; PMID:18632683; http://dx.doi.org/10.1093/hmg/ddn201
18. Angelucci F, Brenè S, Mathé AA. BDNF in schizophrenia, depression and corresponding animal models. Mol Psychiatry 2005; 10:345-52; PMID:15655562; http://dx.doi.org/10.1038/sj.mp.4001637
19. Martinez I, Cazalla D, Almstead LL, Steitz JA, DiMaio D. miR-29 and miR-30 regulate B-Myb expression during cellular senescence. Proc Natl Acad Sci U S A 2011; 108:522-7; PMID:21187425; http://dx.doi.org/10.1073/pnas.1017346108
20. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672-6; PMID:10604474; http://dx.doi.org/10.1038/45257
21. Jaeger PA, Wyss-Coray T. Beclin 1 complex in autophagy and Alzheimer disease. Arch Neurol 2010; 67:1181-4; PMID:20937944; http://dx.doi.org/10.1001/ archneurol.2010.258
22. Miracco C, Cosci E, Oliveri G, Luzi P, Pacenti L, Monciatti I, et al. Protein and mRNA expression of autophagy gene Beclin 1 in human brain tumours. Int J Oncol 2007; 30:429-36; PMID:17203225
23. Taulli R, Bersani F, Foglizzo V, Linari A, Vigna E, Ladanyi M, et al. The muscle-specific microRNA miR-206 blocks human rhabdomyosarcoma growth in xenotransplanted mice by promoting myogenic differentiation. J Clin Invest 2009; 119:2366-78; PMID:19620785
24. Yan D, Dong XdaE, Chen X, Wang L, Lu C, Wang J, et al. MicroRNA-1/206 targets c-Met and inhibits rhabdomyosarcoma development. J Biol Chem 2009; 284:29596-604; PMID:19710019; http://dx.doi.org/10.1074/jbc.M109.020511
25. Rosenberg MI, Georges SA, Asawachaicharn A, Analau E, Tapscott SJ. MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J Cell Biol 2006; 175:77-85; PMID:17030984; http://dx.doi.org/10.1083/jcb.200603039
26. Kondo N, Toyama T, Sugiura H, Fujii Y, Yamashita H. miR-206 Expression is down-regulated in estrogen receptor alpha-positive human breast cancer. Cancer Res 2008; 68:5004-8; PMID:18593897; http://dx.doi.org/10.1158/0008-5472.CAN-08- 0180
27. Adams BD, Furneaux H, White BA. The microribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-alpha (ERalpha) and represses ERalpha messenger RNA and protein expression in breast cancer cell lines. Mol Endocrinol 2007; 21:1132-47; PMID:17312270; http://dx.doi.org/10.1210/me.2007-0022
28. Adams BD, Cowee DM, White BA. The role of miR-206 in the epidermal growth factor (EGF) induced repression of estrogen receptor-alpha (ERalpha) signaling and a luminal phenotype in MCF-7 breast cancer cells. Mol Endocrinol 2009; 23:1215-30; PMID:19423651; http://dx.doi.org/10.1210/me.2009-0062
29. Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K, Newman MA, et al. microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 2007; 8:R27; PMID:17326821; http://dx.doi.org/10.1186/gb-2007-8-2-r27
30. Guo LM, Pu Y, Han Z, Liu T, Li YX, Liu M, et al. MicroRNA-9 inhibits ovarian cancer cell growth through regulation of NF-kappaB1. FEBS J 2009; 276:5537-46; PMID:19702828; http://dx.doi.org/10.1111/j.1742-4658.2009.07237.x
31. Luo H, Zhang H, Zhang Z, Zhang X, Ning B, Guo J, et al. Down-regulated miR-9 and miR-433 in human gastric carcinoma. J Exp Clin Cancer Res 2009; 28:82; PMID:19531230; http://dx.doi.org/10.1186/1756-9966-28-82
32. Hu X, Schwarz JK, Lewis JS, Jr., Huettner PC, Rader JS, Deasy JO, et al. A microRNA expression signature for cervical cancer prognosis. Cancer Res 2010; 70:1441-8; PMID:20124485; http://dx.doi.org/10.1158/0008-5472.CAN-09-3289
33. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010; 12:247-56; PMID:20173740
34. Roccaro AM, Sacco A, Chen C, Runnels J, Leleu X, Azab F, et al. microRNA expression in the biology, prognosis, and therapy of Waldenström macroglobulinemia. Blood 2009; 113:4391-402; PMID:19074725; http://dx.doi.org/ 10.1182/blood-2008-09-178228
35. Roccaro AM, Sacco A, Jia X, Azab AK, Maiso P, Ngo HT, et al. microRNA-dependent modulation of histone acetylation in Waldenstrom macroglobulinemia. Blood 2010; 116:1506-14; PMID:20519629; http://dx.doi.org/10. 1182/blood-2010-01-265686
36. Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell 2007; 128:669-81; PMID:17320505; http://dx.doi.org/10.1016/j.cell.2007.01. 033
37. Shao Y, Gao Z, Marks PA, Jiang X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci U S A 2004; 101:18030-5; PMID:15596714; http://dx.doi.org/10.1073/pnas.0408345102
38. Cao DJ, Wang ZV, Battiprolu PK, Jiang N, Morales CR, Kong Y, et al. Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci U S A 2011; 108:4123-8; PMID:21367693; http://dx.doi.org/10.1073/pnas.1015081108
39. Buechner J, Tømte E, Haug BH, Henriksen JR, Løkke C, Flægstad T, et al. Tumour-suppressor microRNAs let-7 and mir-101 target the proto-oncogene MYCN and inhibit cell proliferation in MYCN-amplified neuroblastoma. Br J Cancer 2011; 105:296-303; PMID:21654684; http://dx.doi.org/10.1038/bjc.2011.220
40. Li S, Fu H, Wang Y, Tie Y, Xing R, Zhu J, et al. MicroRNA-101 regulates expression of the v-fos FBJ murine osteosarcoma viral oncogene homolog (FOS) oncogene in human hepatocellular carcinoma. Hepatology 2009; 49:1194-202; PMID:19133651; http://dx.doi.org/10.1002/hep.22757
41. Sachdeva M, Wu H, Ru P, Hwang L, Trieu V, Mo YY. MicroRNA-101-mediated Akt activation and estrogen-independent growth. Oncogene 2011; 30:822-31; PMID:20956939; http://dx.doi.org/10.1038/onc.2010.463
42. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y, et al. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 2009; 69:1135-42; PMID:19155302; http://dx.doi.org/ 10.1158/0008-5472.CAN-08-2886
43. Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B, et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 2008; 322:1695-9; PMID:19008416; http://dx.doi.org/10.1126/ science.1165395
44. Zhang JG, Guo JF, Liu DL, Liu Q, Wang JJ. MicroRNA-101 exerts tumor-suppressive functions in non-small cell lung cancer through directly targeting enhancer of zeste homolog 2. J Thorac Oncol 2011; 6:671-8; PMID:21270667; http://dx.doi.org/10.1097/JTO.0b013e318208eb35
45. Frankel LB, Wen J, Lees M, Høyer-Hansen M, Farkas T, Krogh A, et al. microRNA-101 is a potent inhibitor of autophagy. EMBO J 2011; 30:4628-41; PMID:21915098; http://dx.doi.org/10.1038/emboj.2011.331
46. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, et al. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992; 70:715-28; PMID:1516130; http://dx.doi.org/10.1016/0092- 8674(92)90306-W
47. Ravikumar B, Imarisio S, Sarkar S, O'Kane CJ, Rubinsztein DC. Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J Cell Sci 2008; 121:1649-60; PMID:18430781; http://dx.doi.org/10.1242/jcs.025726
48. Mariño G, Uría JA, Puente XS, Quesada V, Bordallo J, López-Otín C. Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem 2003; 278:3671-8; PMID:12446702; http://dx.doi.org/10.1074/jbc.M208247200
49. Li M, Hou Y, Wang J, Chen X, Shao ZM, Yin XM. Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. J Biol Chem 2011; 286:7327-38; PMID:21177865; http://dx.doi.org/10. 1074/jbc.M110.199059
50. Gavet O, Ozon S, Manceau V, Lawler S, Curmi P, Sobel A. The stathmin phosphoprotein family: intracellular localization and effects on the microtubule network. J Cell Sci 1998; 111:3333-46; PMID:9788875
51. Rana S, Maples PB, Senzer N, Nemunaitis J. Stathmin 1: a novel therapeutic target for anticancer activity. Expert Rev Anticancer Ther 2008; 8:1461-70; PMID:18759697; http://dx.doi.org/10.1586/14737140.8.9.1461
52. Phadke AP, Jay CM, Wang Z, Chen S, Liu S, Haddock C, et al. In vivo safety and antitumor efficacy of bifunctional small hairpin RNAs specific for the human Stathmin 1 oncoprotein. DNA Cell Biol 2011; 30:715-26; PMID:21612405; http://dx.doi.org/10.1089/dna.2011.1240
53. Alli E, Yang JM, Hait WN. Silencing of stathmin induces tumor-suppressor function in breast cancer cell lines harboring mutant p53. Oncogene 2007; 26:1003-12; PMID:16909102; http://dx.doi.org/10.1038/sj.onc.1209864
54. Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, et al. Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res 2004; 64:3087-95; PMID:15126345; http://dx.doi.org/10.1158/0008-5472.CAN-03-3773
55. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65:9628-32; PMID:16266980; http://dx.doi.org/10.1158/0008-5472.CAN-05-2352
56. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, et al. A microRNA polycistron as a potential human oncogene. Nature 2005; 435:828-33; PMID:15944707; http://dx.doi.org/10.1038/nature03552
57. Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res 2008; 68:8191-4; PMID:18922889; http://dx.doi.org/10.1158/0008-5472.CAN-08- 1768
58. Meenhuis A, van Veelen PA, de Looper H, van Boxtel N, van den Berge IJ, Sun SM, et al. MiR-17/20/93/106 promote hematopoietic cell expansion by targeting sequestosome 1-regulated pathways in mice. Blood 2011; 118:916-25; PMID:21628417; http://dx.doi.org/10.1182/blood-2011-02-336487
59. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131:1149-63; PMID:18083104; http://dx.doi.org/10.1016/j.cell.2007.10.035
60. Moscat J, Diaz-Meco MT. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 2009; 137:1001-4; PMID:19524504; http://dx.doi.org/10.1016/j. cell.2009.05.023
61. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009; 137:1062-75; PMID:19524509; http://dx.doi.org/10.1016/j.cell.2009.03.048
62. Courboulin A, Paulin R, Giguère NJ, Saksouk N, Perreault T, Meloche J, et al. Role for miR-204 in human pulmonary arterial hypertension. J Exp Med 2011; 208:535-48; PMID:21321078; http://dx.doi.org/10.1084/jem.20101812
63. Wang FE, Zhang C, Maminishkis A, Dong L, Zhi C, Li R, et al. MicroRNA-204/211 alters epithelial physiology. FASEB J 2010; 24:1552-71; PMID:20056717; http://dx.doi.org/10.1096/fj.08-125856
64. Jian X, Xiao-yan Z, Bin H, Yu-feng Z, Bo K, Zhi-nong W, et al. MiR-204 regulate cardiomyocyte autophagy induced by hypoxia-reoxygenation through LC3-II. Int J Cardiol 2011; 148:110-2; PMID:21316776; http://dx.doi.org/10.1016/ j.ijcard.2011.01.029
65. Yekta S, Shih IH, Bartel DP. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004; 304:594-6; PMID:15105502; http://dx.doi.org/10.1126/science. 1097434
66. Hornstein E, Mansfield JH, Yekta S, Hu JK, Harfe BD, McManus MT, et al. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 2005; 438:671-4; PMID:16319892; http://dx.doi.org/10.1038/nature04138
67. Mueller DW, Bosserhoff AK. MicroRNA miR-196a controls melanoma-associated genes by regulating HOX-C8 expression. Int J Cancer 2011; 129:1064-74; PMID:21077158; http://dx.doi.org/10.1002/ijc.25768
68. Coskun E, von der Heide EK, Schlee C, Kühnl A, Gökbuget N, Hoelzer D, et al. The role of microRNA-196a and microRNA-196b as ERG regulators in acute myeloid leukemia and acute T-lymphoblastic leukemia. Leuk Res 2011; 35:208-13; PMID:20570349; http://dx.doi.org/10.1016/j.leukres.2010.05.007
69. Hu Z, Shu Y, Chen Y, Chen J, Dong J, Liu Y, et al. Genetic polymorphisms in the precursor MicroRNA flanking region and non-small cell lung cancer survival. Am J Respir Crit Care Med 2011; 183:641-8; PMID:20889907; http://dx.doi.org/10.1164/rccm.201005-0717OC
70. Xu W, Xu J, Liu S, Chen B, Wang X, Li Y, et al. Effects of common polymorphisms rs11614913 in miR-196a2 and rs2910164 in miR-146a on cancer susceptibility: a meta-analysis. PLoS One 2011; 6:e20471; PMID:21637771; http://dx.doi.org/10.1371/journal.pone.0020471
71. Christensen BC, Avissar-Whiting M, Ouellet LG, Butler RA, Nelson HH, McClean MD, et al. Mature microRNA sequence polymorphism in MIR196A2 is associated with risk and prognosis of head and neck cancer. Clin Cancer Res 2010; 16:3713-20; PMID:20501619; http://dx.doi.org/10.1158/1078-0432.CCR-10-0657
72. Brest P, Corcelle EA, Cesaro A, Chargui A, Belaïd A, Klionsky DJ, et al. Autophagy and Crohn's disease: at the crossroads of infection, inflammation, immunity, and cancer. Curr Mol Med 2010; 10:486-502; PMID:20540703; http://dx.doi.org/10.2174/156652410791608252
73. Brest P, Lapaquette P, Souidi M, Lebrigand K, Cesaro A, Vouret-Craviari V, et al. A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease. Nat Genet 2011; 43:242-5; PMID:21278745; http://dx.doi.org/10.1038/ng.762
74. Singh SB, Ornatowski W, Vergne I, Naylor J, Delgado M, Roberts E, et al. Human IRGM regulates autophagy and cell-autonomous immunity functions through mitochondria. Nat Cell Biol 2010; 12:1154-65; PMID:21102437; http://dx.doi.org/10.1038/ncb2119
75. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9:47-59; PMID:18097445; http://dx.doi.org/10.1038/nrm2308
76. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8:741-52; PMID:17717517; http://dx.doi.org/10.1038/nrm2239
77. Kroemer G, Mariño G, Levine B.. Autophagy and the integrated stress response. Mol Cell 2010; 40:280-93; PMID:20965422; http://dx.doi.org/10.1016/j. molcel.2010.09.023
78. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 2007; 26:2527-39; PMID:17446862; http://dx.doi.org/10.1038/sj. emboj.7601689
79. Germain M, Nguyen AP, Le Grand JN, Arbour N, Vanderluit JL, Park DS, et al. MCL-1 is a stress sensor that regulates autophagy in a developmentally regulated manner. EMBO J 2011; 30:395-407; PMID:21139567; http://dx.doi.org/10. 1038/emboj.2010.327
80. Luo S, Rubinsztein DC. Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL. Cell Death Differ 2010; 17:268-77; PMID:19713971; http://dx.doi.org/10.1038/cdd.2009.121
81. 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; 102:13944-9; PMID:16166262; http://dx.doi.org/10.1073/pnas.0506654102
82. Xu J, Liao X, Wong C. Downregulations of B-cell lymphoma 2 and myeloid cell leukemia sequence 1 by microRNA 153 induce apoptosis in a glioblastoma cell line DBTRG-05MG. Int J Cancer 2010; 126:1029-35; PMID:19676043
83. Jin Z, Li Y, Pitti R, Lawrence D, Pham VC, Lill JR, et al. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 2009; 137:721-35; PMID:19427028; http://dx.doi.org/10. 1016/j.cell.2009.03.015
84. Gao Z, Gammoh N, Wong PM, Erdjument-Bromage H, Tempst P, Jiang X. Processing of autophagic protein LC3 by the 20S proteasome.. Autophagy 2010; 6:126-37; PMID:20061800; http://dx.doi.org/10.4161/auto.6.1.10928
85. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, et al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8:1124-32; PMID:16998475; http://dx.doi.org/10.1038/ncb1482
86. Cheng Y, Ren X, Zhang Y, Patel R, Sharma A, Wu H, et al. eEF-2 kinase dictates cross-talk between autophagy and apoptosis induced by Akt Inhibition, thereby modulating cytotoxicity of novel Akt inhibitor MK-2206. Cancer Res 2011; 71:2654-63; PMID:21307130; http://dx.doi.org/10.1158/0008-5472.CAN-10-2889
87. Chen L, Yan HX, Yang W, Hu L, Yu LX, Liu Q, et al. The role of microRNA expression pattern in human intrahepatic cholangiocarcinoma. J Hepatol 2009; 50:358-69; PMID:19070389; http://dx.doi.org/10.1016/j.jhep.2008.09.015
88. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455:64-71; PMID:18668037; http://dx.doi.org/10.1038/nature07242
89. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008; 455:58-63; PMID:18668040; http://dx.doi.org/10.1038/nature07228
90. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH, et al. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res 2009; 37:1672-81; PMID:19153141; http://dx.doi.org/10.1093/nar/gkp002
91. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 2010; 465:1033-8; PMID:20577206; http://dx.doi.org/10.1038/ nature09144
92. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG, et al. In vivo identification of tumor- suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 2011; 147:382-95; PMID:22000016; http://dx.doi.org/10.1016/j.cell.2011.09.032
93. Tay Y, Kats L, Salmena L, Weiss D, Tan SM, Ala U, et al. Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 2011; 147:344-57; PMID:22000013; http://dx.doi.org/10. 1016/j.cell.2011.09.029
94. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011; 147:358-69; PMID:22000014; http://dx.doi.org/10.1016/j.cell.2011.09.028
95. Sumazin P, Yang X, Chiu HS, Chung WJ, Iyer A, Llobet-Navas D, et al. An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 2011; 147:370-81; PMID:22000015; http://dx.doi.org/10.1016/j.cell.2011.09.041
96. Tian Y, Li Z, Hu W, Ren H, Tian E, Zhao Y, et al. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell 2010; 141:1042-55; PMID:20550938; http://dx.doi.org/10.1016/j.cell.2010.04.034
97. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 2011; 146:353-8; PMID:21802130; http://dx.doi.org/10.1016/j.cell.2011.07.014
98. Jegga AG, Schneider L, Ouyang X, Zhang J. Systems biology of the autophagy-lysosomal pathway.. Autophagy 2011; 7:477-89; PMID:21293178; http://dx.doi.org/10.4161/auto.7.5.14811
99. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013
100. Korkmaz G, le Sage C, Tekirdag KA, Agami R, Gozuacik D. miR-376b controls starvation and mTOR inhibition-related autophagy by targeting ATG4C and BECN1. Autophagy 2012; In press; PMID:22248718