MicroRNAs in apoptosis, autophagy and necroptosis

Oncotarget

Volumn 6, Issue 11, 2015, Pages 8474-8490

  Su, Zhenyi ^a,b   Yang, Zuozhang ^c,d   Xu, Yongqing ^d   Chen, Yongbin ^e   Yu, Qiang ^f  

^a SOUTHEAST UNIVERSITY   (China)

^b HARVARD MEDICAL SCHOOL   (United States)

^c KUNMING MEDICAL UNIVERSITY   (China)

^d KUNMING GENERAL HOSPITAL   (China)

^e KUNMING INSTITUTE OF ZOOLOGY   (China)

^f SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

Apoptosis; Autophagy; Cancer progression; microRNA; Necroptosis

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BIM PROTEIN; CASPASE 3; CASPASE 6; CASPASE 7; CASPASE 9; CYTOCHROME C; DEATH ASSOCIATED PROTEIN KINASE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; FLICE INHIBITORY PROTEIN; GUANOSINE TRIPHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; KRUPPEL LIKE FACTOR 4; MASPIN; MICRORNA; MICRORNA 155; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN BCL XL; PROTEIN BID; PROTEIN MCL 1; RAS PROTEIN; SMAD PROTEIN; TUBERIN; TUMOR NECROSIS FACTOR ALPHA; UNTRANSLATED RNA; APOPTOSIS REGULATORY PROTEIN; DEATH RECEPTOR; MESSENGER RNA; RNA; TUMOR PROTEIN;

3' UNTRANSLATED REGION; ACUTE MYELOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER GROWTH; CELL DEATH; CONTROLLED STUDY; DEFENSE MECHANISM; HUMAN; HUMAN CELL; NECROPTOSIS; OSTEOSARCOMA CELL; PROTEIN EXPRESSION; RNA CLEAVAGE; TUMOR GROWTH; ANIMAL; DISEASE COURSE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NECROSIS; NEOPLASM; PATHOLOGY; PHAGOSOME; PHYSIOLOGY; RNA STABILITY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; DISEASE PROGRESSION; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NECROSIS; NEOPLASM PROTEINS; NEOPLASMS; PHAGOSOMES; RECEPTORS, DEATH DOMAIN; RNA STABILITY; RNA, MESSENGER; RNA, NEOPLASM; SIGNAL TRANSDUCTION;

EID: 84928751178     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3523     Document Type: Article

References (146)

1. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szász AM, Wang ZC, Brock JE, Richardson AL, Weinberg RA. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell. 2009; 137:1032-1046.
2. Png KJ, Halberg N, Yoshida M, Tavazoie SF. A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature. 2012; 481:190-194.
3. Sanchez-Diaz PC, Hsiao T-H, Zou Y, Sugalski AJ, Heim-Hall J, Chen Y, Langevin A-M, Hung JY. In silico functional analyses and discovery of survival-associated microRNA signatures in pediatric osteosarcoma. Oncoscience. 2014; 1:599.
4. Ninio-Many L, Grossman H, Levi M, Zilber S, Tsarfaty I, Shomron N, Tuvar A, Chuderland D, Stemmer SM, Ben-Aharon I. MicroRNA miR-125a-3p modulates molecular pathway of motility and migration in prostate cancer cells. Oncoscience. 2014; 1:250.
5. Martin EC, Krebs AE, Burks HE, Elliott S, Baddoo M, Collins-Burow BM, Flemington EK, Burow ME. miR-155 induced transcriptome changes in the MCF-7 breast cancer cell line leads to enhanced mitogen activated protein kinase signaling. Genes & cancer. 2014; 5:353.
6. Li H, Gupta S, Du WW, Yang BB. MicroRNA-17 inhibits tumor growth by stimulating T-cell mediated host immune response. Oncoscience. 2014; 1:531.
7. Dontula R, Dinasarapu A, Chetty C, Pannuru P, Herbert E, Ozer H, Lakka SS. MicroRNA 203 modulates glioma cell migration via Robo1/ERK/MMP-9 signaling. Genes & cancer. 2013; 1947601913500141.
8. Li H, Yang BB. MicroRNA in drug resistance. Oncoscience. 2014; 1:3-4.
9. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nature Reviews Genetics. 2010; 11:597-610.
10. Huang Y, Shen XJ, Zou Q, Wang SP, Tang SM, Zhang GZ. Biological functions of microRNAs: a review. Journal of physiology and biochemistry. 2011; 67:129-139.
11. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell. 2009; 136:642-655.
12. Alahari SK. Regulation of Metastasis by miRNAs. MicroRNA in Cancer: Springer. 2013; :81-95.
13. Verbrugge I, Johnstone RW, Smyth MJ. SnapShot: extrinsic apoptosis pathways. Cell. 2010; 143:1192-1192. e1192.
14. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol. 2011; 13:184-190.
15. Srivastava R. Apoptosis, Cell Signaling, and Human Diseases: Springer 2007.
16. Lima RT, Busacca S, Almeida GM, Gaudino G, Fennell DA, Vasconcelos MH. MicroRNA regulation of core apoptosis pathways in cancer. Eur J Cancer. 2011; 47:163-174.
17. Zuckerman V, Wolyniec K, Sionov RV, Haupt S, Haupt Y. Tumour suppression by p53: the importance of apoptosis and cellular senescence. The Journal of pathology. 2009; 219:3-15.
18. Hamada S, Masamune A, Miura S, Satoh K, Shimosegawa T. MiR-365 induces gemcitabine resistance in pancreatic cancer cells by targeting the adaptor protein SHC1 and pro-apoptotic regulator BAX. Cell Signal. 2014; 26:179-185.
19. Zhou M, Liu Z, Zhao Y, Ding Y, Liu H, Xi Y, Xiong W, Li G, Lu J, Fodstad O. MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist killer 1 (Bak1) expression. J Biol Chem. 2010; 285:21496-21507.
20. Nakano H, Miyazawa T, Kinoshita K, Yamada Y, Yoshida T. Functional screening identifies a microRNA, miR-491 that induces apoptosis by targeting Bcl-XL in colorectal cancer cells. Int J Cancer. 2010; 127:1072-1080.
21. Ji F, Zhang H, Wang Y, Li M, Xu W, Kang Y, Wang Z, Wang Z, Cheng P, Tong D. MicroRNA-133a, downregulated in osteosarcoma, suppresses proliferation and promotes apoptosis by targeting Bcl-xL and Mcl-1. Bone. 2013; 56:220-226.
22. Zhang Y, Schiff D, Park D, Abounader R. MicroRNA-608 and MicroRNA-34a Regulate Chordoma Malignancy by Targeting EGFR, Bcl-xL and MET. PloS one. 2014; 9:e91546.
23. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102:13944-13949.
24. Sacconi A, Biagioni F, Canu V, Mori F, Di Benedetto A, Lorenzon L, Ercolani C, Di Agostino S, Cambria A, Germoni S. miR-204 targets Bcl-2 expression and enhances responsiveness of gastric cancer. Cell Death & Disease. 2012; 3:e423.
25. Zhang H, Li Y, Huang Q, Ren X, Hu H, Sheng H, Lai M. MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death & Differentiation. 2011; 18:1702-1710.
26. Srivastava N, Manvati S, Srivastava A, Pal R, Kalaiarasan P, Chattopadhyay S, Gochhait S, Dua R, Bamezai R. miR-24-2 controls H2AFX expression regardless of gene copy number alteration and induces apoptosis by targeting antiapoptotic gene BCL-2: a potential for therapeutic intervention. Breast Cancer Res. 2011; 13:R39.
27. Chen Q, Xu J, Li L, Li H, Mao S, Zhang F, Zen K, Zhang C, Zhang Q. MicroRNA-23a/b and microRNA-27a/b suppress Apaf-1 protein and alleviate hypoxia-induced neuronal apoptosis. Cell Death & Disease. 2014; 5:e1132.
28. Xu C, Lu Y, Pan Z, Chu W, Luo X, Lin H, Xiao J, Shan H, Wang Z, Yang B. The muscle-specific microRNAs miR-1 and miR-133 produce opposing effects on apoptosis by targeting HSP60, HSP70 and caspase-9 in cardiomyocytes. J Cell Sci. 2007; 120:3045-3052.
29. Walker JC, Harland RM. microRNA-24a is required to repress apoptosis in the developing neural retina. Genes Dev. 2009; 23:1046-1051.
30. Wang P, Zhuang L, Zhang J, Fan J, Luo J, Chen H, Wang K, Liu L, Chen Z, Meng Z. The serum miR-21 level serves as a predictor for the chemosensitivity of advanced pancreatic cancer, and miR-21 expression confers chemoresistance by targeting FasL. Molecular oncology. 2013; 7:334-345.
31. Shaffiey F, Cross E, Sathyanarayana P. Mir-590 Is a Novel STAT5 Regulated Oncogenic miRNA and Targets FasL In Acute Myeloid Leukemia. Blood. 2013; 122:3811-3811.
32. Huang G, Nishimoto K, Zhou Z, Hughes D, Kleinerman ES. miR-20a encoded by the miR-17-92 cluster increases the metastatic potential of osteosarcoma cells by regulating Fas expression. Cancer Res. 2012; 72:908-916.
33. Guo Q, Zhang J, Li J, Zou L, Zhang J, Xie Z, Fu X, Jiang S, Chen G, Jia Q. Forced miR-146a expression causes autoimmune lymphoproliferative syndrome in mice via downregulation of Fas in germinal center B cells. Blood. 2013; 121:4875-4883.
34. Li Z, Huang H, Chen P, He M, Li Y, Arnovitz S, Jiang X, He C, Hyjek E, Zhang J. miR-196b directly targets both HOXA9/MEIS1 oncogenes and FAS tumour suppressor in MLL-rearranged leukaemia. Nature Communications. 2012; 2:688.
35. Razumilava N, Bronk SF, Smoot RL, Fingas CD, Werneburg NW, Roberts LR, Mott JL. miR-25 targets TNFrelated apoptosis inducing ligand (TRAIL) death receptor-4 and promotes apoptosis resistance in cholangiocarcinoma. Hepatology. 2012; 55:465-475.
36. Abend JR, Uldrick T, Ziegelbauer JM. Regulation of tumor necrosis factor-like weak inducer of apoptosis receptor protein (TWEAKR) expression by Kaposi's sarcoma-associated herpesvirus microRNA prevents TWEAK-induced apoptosis and inflammatory cytokine expression. J Virol. 2010; 84:12139-12151.
37. Zhang L, Dong L, Li Y, Hong Z, Wei W. The microRNA miR-181c controls microglia-mediated neuronal apoptosis by suppressing tumor necrosis factor. Journal of neuroinflammation. 2012; 9:211.
38. Rossato M, Curtale G, Tamassia N, Castellucci M, Mori L, Gasperini S, Mariotti B, De Luca M, Mirolo M, Cassatella MA. IL-10-induced microRNA-187 negatively regulates TNF-α, IL-6, and IL-12p40 production in TLR4-stimulated monocytes. Proceedings of the National Academy of Sciences. 2012; 109:E3101-E3110.
39. Guennewig B, Roos M, Dogar AM, Gebert LF, Zagalak JA, Vongrad V, Metzner KJ, Hall J. Synthetic pre-microRNAs reveal dual-strand activity of miR-34a on TNF-α. RNA. 2014; 20:61-75.
40. Wang HQ, Yu XD, Liu ZH, Cheng X, Samartzis D, Jia LT, Wu SX, Huang J, Chen J, Luo ZJ. Deregulated miR-155 promotes Fas-mediated apoptosis in human intervertebral disc degeneration by targeting FADD and caspase-3. The Journal of pathology. 2011; 225:232-242.
41. Yamada N, Noguchi S, Kumazaki M, Shinohara H, Miki K, Naoe T, Akao Y. Epigenetic regulation of microRNA-128a expression contributes to the apoptosis-resistance of human T-cell leukaemia Jurkat cells by modulating expression of Fas-associated protein with death domain (FADD). Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 2014; 1843:590-602.
42. Wang K, Liu F, Zhou L, Ding S, Long B, Liu C, Sun T, Fan Y, Sun L, Li P. miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death & Disease. 2013; 4:e709.
43. Zhang J, Du Y, Wu C, Ren X, Ti X, Shi J, Zhao F, Yin H. Curcumin promotes apoptosis in human lung adenocarcinoma cells through miR-186* signaling pathway. Oncol Rep. 2010; 24:1217-1223.
44. Chen F, Zhu H-H, Zhou L-F, Wu S-S, Wang J, Chen Z. Inhibition of c-FLIP expression by miR-512-3p contributes to taxol-induced apoptosis in hepatocellular carcinoma cells. Oncol Rep. 2010; 23:1457-1462.
45. Chitnis NS, Pytel D, Bobrovnikova-Marjon E, Pant D, Zheng H, Maas NL, Frederick B, Kushner JA, Chodosh LA, Koumenis C. miR-211 Is a Prosurvival MicroRNA that Regulates chop Expression in a PERK-Dependent Manner. Mol Cell. 2012; 48:353-364.
46. Behrman S, Acosta-Alvear D, Walter P. A CHOP-regulated microRNA controls rhodopsin expression. The Journal of Cell Biology. 2011; 192:919-927.
47. Tsang WP, Kwok TT. Let-7a microRNA suppresses therapeutics- induced cancer cell death by targeting caspase-3. Apoptosis. 2008; 13:1215-1222.
48. Fang J, Song X-W, Tian J, Chen H-Y, Li D-F, Wang J-F, Ren A-J, Yuan W-J, Lin L. Overexpression of microRNA-378 attenuates ischemia-induced apoptosis by inhibiting caspase-3 expression in cardiac myocytes. Apoptosis. 2012; 17:410-423.
49. Hudson R, Yi M, Esposito D, Glynn S, Starks A, Yang Y, Schetter A, Watkins S, Hurwitz A, Dorsey T. MicroRNA-106b-25 cluster expression is associated with early disease recurrence and targets caspase-7 and focal adhesion in human prostate cancer. Oncogene. 2013; 32:4139-4147.
50. Chen H-Y, Lin Y-M, Chung H-C, Lang Y-D, Lin C-J, Huang J, Wang W-C, Lin F-M, Chen Z, Huang H-D. miR-103/107 promote metastasis of colorectal cancer by targeting the metastasis suppressors DAPK and KLF4. Cancer Res. 2012; 72:3631-3641.
51. Li Q, Zhang D, Wang Y, Sun P, Hou X, Larner J, Xiong W, Mi J. MiR-21/Smad 7 signaling determines TGF-β1- induced CAF formation. Scientific reports. 2013; 3.
52. Lan SH, Wu SY, Zuchini R, Lin XZ, Su IJ, Tsai TF, Lin YJ, Wu CT, Liu HS. Autophagy suppresses tumorigenesis of hepatitis B virus-associated hepatocellular carcinoma through degradation of microRNA-224. Hepatology. 2014; 59:505-517.
53. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, Lim B. MicroRNA-125b is a novel negative regulator of p53. Genes Dev. 2009; 23:862-876.
54. Swarbrick A, Woods SL, Shaw A, Balakrishnan A, Phua Y, Nguyen A, Chanthery Y, Lim L, Ashton LJ, Judson RL. miR-380-5p represses p53 to control cellular survival and is associated with poor outcome in MYCN-amplified neuroblastoma. Nat Med. 2010; 16:1134-1140.
55. Hu W, Chan CS, Wu R, Zhang C, Sun Y, Song JS, Tang LH, Levine AJ, Feng Z. Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol Cell. 2010; 38:689-699.
56. Xu C-X, Xu M, Tan L, Yang H, Permuth-Wey J, Kruk PA, Wenham RM, Nicosia SV, Lancaster JM, Sellers TA. MicroRNA miR-214 regulates ovarian cancer cell stemness by targeting p53/Nanog. J Biol Chem. 2012; 287:34970-34978.
57. Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet. 2010; 6:e1000795.
58. Ye D, Wang G, Liu Y, Huang W, Wu M, Zhu S, Jia W, Deng AM, Liu H, Kang J. MiR-138 Promotes Induced Pluripotent Stem Cell Generation Through the Regulation of the p53 Signaling. Stem Cells. 2012; 30:1645-1654.
59. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K. Modulation of microRNA processing by p53. Nature. 2009; 460:529-533.
60. Jin L, Hu WL, Jiang CC, Wang JX, Han CC, Chu P, Zhang LJ, Thorne RF, Wilmott J, Scolyer RA. MicroRNA-149*, a p53-responsive microRNA, functions as an oncogenic regulator in human melanoma. Proceedings of the National Academy of Sciences. 2011; 108:15840-15845.
61. Barlev N, Sayan B, Candi E, Okorokov A. The microRNA and p53 families join forces against cancer. Cell Death & Differentiation. 2010; 17:373-375.
62. Donzelli S, Strano S, Blandino G. microRNAs: short noncoding bullets of gain of function mutant p53 proteins. Oncoscience. 2014; 1:427.
63. 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. Proceedings of the National Academy of Sciences. 2011; 108:11662-11667.
64. Xie Y, Tobin LA, Camps J, Wangsa D, Yang J, Rao M, Witasp E, Awad KS, Yoo N, Ried T. MicroRNA-24 regulates XIAP to reduce the apoptosis threshold in cancer cells. Oncogene. 2013; 32:2442-2451.
65. Bian K, Fan J, Zhang X, Yang X-W, Zhu H-Y, Wang L, Sun J-Y, Meng Y-L, Cui P-C, Cheng S-Y. MicroRNA-203 leads to G1 phase cell cycle arrest in laryngeal carcinoma cells by directly targeting survivin. FEBS Lett. 2012; 586:804-809.
66. Alajez NM, Lenarduzzi M, Ito E, Hui AB, Shi W, Bruce J, Yue S, Huang SH, Xu W, Waldron J. MiR-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway. Cancer Res. 2011; 71:2381-2391.
67. Keklikoglou I, Koerner C, Schmidt C, Zhang J, Heckmann D, Shavinskaya A, Allgayer H, Gückel B, Fehm T, Schneeweiss A. MicroRNA-520/373 family functions as a tumor suppressor in estrogen receptor negative breast cancer by targeting NF-κB and TGF-β signaling pathways. Oncogene. 2012; 31:4150-4163.
68. Jiang L, Lin C, Song L, Wu J, Chen B, Ying Z, Fang L, Yan X, He M, Li J. MicroRNA-30e* promotes human glioma cell invasiveness in an orthotopic xenotransplantation model by disrupting the NF-κB/IκBα negative feedback loop. The Journal of clinical investigation. 2012; 122:33.
69. Ding J, Huang S, Wang Y, Tian Q, Zha R, Shi H, Wang Q, Ge C, Chen T, Zhao Y. Genome-wide screening reveals that miR-195 targets the TNF-α/NF-κB pathway by downregulating IκB kinase alpha and TAB3 in hepatocellular carcinoma. Hepatology. 2013; 58:654-666.
70. Legakis JE, Yen W, Klionsky DJ. A cycling protein complex required for selective autophagy. Autophagy. 2007; 3:422.
71. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol. 2010; 22:124-131.
72. Ichimura Y, Komatsu M. Selective degradation of p62 by autophagy. Seminars in immunopathology. Springer 2010; :431-436.
73. Frankel LB, Lund AH. MicroRNA regulation of autophagy. Carcinogenesis. 2012; 33:2018-2025.
74. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010; 40:280-293.
75. Singh R, Cuervo AM. Autophagy in the cellular energetic balance. Cell metabolism. 2011; 13:495-504.
76. Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Molecular biology of the cell. 2008; 19:2092-2100.
77. Wang S-y, Yu Q-j, Zhang R-d, Liu B. Core signaling pathways of survival/death in autophagy-related cancer networks. The international journal of biochemistry & cell biology. 2011; 43:1263-1266.
78. Lorin S, Hamaï A, Mehrpour M, Codogno P. Autophagy regulation and its role in cancer. Semin Cancer Biol. Elsevier 2013; :361-379.
79. Meijer AJ, Codogno P. Autophagy: regulation by energy sensing. Curr Biol. 2011; 21:R227-R229.
80. Maiuri MC, Galluzzi L, Morselli E, Kepp O, Malik SA, Kroemer G. Autophagy regulation by p53. Curr Opin Cell Biol. 2010; 22:181-185.
81. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009; 43:67.
82. Russell RC, Yuan H-X, Guan K-L. Autophagy regulation by nutrient signaling. Cell Res. 2014; 24:42-57.
83. Wu H, Wang F, Hu S, Yin C, Li X, Zhao S, Wang J, Yan X. MiR-20a and miR-106b negatively regulate autophagy induced by leucine deprivation via suppression of ULK1 expression in C2C12 myoblasts. Cell Signal. 2012; 24:2179-2186.
84. Ju J-A, Huang C-T, Lan S-H, Wang T-H, Lin P-C, Lee J-C, Tian Y-F, Liu H-S. Characterization of a colorectal cancer migration and autophagy-related microRNA miR-338-5p and its target gene PIK3C3. Biomarkers and Genomic Medicine. 2013; 5:74-78.
85. Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X, Liu C-G, Yang J-M. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy. 2009; 5:816-823.
86. 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; 8:165-176.
87. Menghini R, Casagrande V, Marino A, Marchetti V, Cardellini M, Stoehr R, Rizza S, Martelli E, Greco S, Mauriello A. MiR-216a: a link between endothelial dysfunction and autophagy. Cell Death & Disease. 2014; 5:e1029.
88. Huang Y, Guerrero-Preston R, Ratovitski EA. Phospho-ΔNp63α-dependent regulation of autophagic signaling through transcription and micro-RNA modulation. Cell Cycle. 2012; 11:1247.
89. Mikhaylova O, Stratton Y, Hall D, Kellner E, Ehmer B, Drew AF, Gallo CA, Plas DR, Biesiada J, Meller J. VHLregulated MiR-204 suppresses tumor growth through inhibition of LC3B-mediated autophagy in renal clear cell carcinoma. Cancer Cell. 2012; 21:532-546.
90. Frankel LB, Wen J, Lees M, Høyer-Hansen M, Farkas T, Krogh A, Jäättelä M, Lund AH. microRNA-101 is a potent inhibitor of autophagy. The EMBO journal. 2011; 30:4628-4641.
91. Comincini S, Allavena G, Palumbo S, Morini M, Durando F, Angeletti F, Pirtoli L, Miracco C. microRNA-17 regulates the expression of ATG7 and modulates the autophagy process, improving the sensitivity to temozolomide and lowdose ionizing radiation treatments in human glioblastoma cells. Cancer biology & therapy. 2013; 14:574-586.
92. Chang Y, Yan W, He X, Zhang L, Li C, Huang H, Nace G, Geller DA, Lin J, Tsung A. miR-375 inhibits autophagy and reduces viability of hepatocellular carcinoma cells under hypoxic conditions. Gastroenterology. 2012; 143:177-187. e178.
93. Wang P, Zhang J, Zhang L, Zhu Z, Fan J, Chen L, Zhuang L, Luo J, Chen H, Liu L. MicroRNA 23b regulates autophagy associated with radioresistance of pancreatic cancer cells. Gastroenterology. 2013; 145:1133-1143. e1112.
94. Lu C, Xu Z-x. MiR-106b family regulates autophagy via targeting ATG16L1. The Journal of Immunology. 2012; 188:172. 141.
95. Yu Y, Cao L, Yang L, Kang R, Lotze M, Tang D. microRNA 30A promotes autophagy in response to cancer therapy. Autophagy. 2012; 8:853-855.
96. Ying Q, Liang L, Guo W, Zha R, Tian Q, Huang S, Yao J, Ding J, Bao M, Ge C. Hypoxia-inducible MicroRNA-210 augments the metastatic potential of tumor cells by targeting vacuole membrane protein 1 in hepatocellular carcinoma. Hepatology. 2011; 54:2064-2075.
97. Zhao G, Zhang J-G, Liu Y, Qin Q, Wang B, Tian K, Liu L, Li X, Niu Y, Deng S-C. MiR-148b functions as a tumor suppressor in pancreatic cancer by targeting AMPKα1. Mol Cancer Ther. 2013; 12:83-93.
98. Zhao N, Wang R, Zhou L, Zhu Y, Gong J, Zhuang S-M. MicroRNA-26b suppresses the NF-κB signaling and enhances the chemosensitivity of hepatocellular carcinoma cells by targeting TAK1 and TAB3. Molecular cancer. 2014; 13:35.
99. Oneyama C, Ikeda J, Okuzaki D, Suzuki K, Kanou T, Shintani Y, Morii E, Okumura M, Aozasa K, Okada M. MicroRNA-mediated downregulation of mTOR/FGFR3 controls tumor growth induced by Src-related oncogenic pathways. Oncogene. 2011; 30:3489-3501.
100. Fornari F, Milazzo M, Chieco P, Negrini M, Calin GA, Grazi GL, Pollutri D, Croce CM, Bolondi L, Gramantieri L. MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res. 2010; 70:5184-5193.
101. Yang Y, Liu L, Zhang Y, Guan H, Wu J, Zhu X, Yuan J, Li M. MiR-503 targets PI3K p85 and IKK-β and suppresses progression of non-small cell lung cancer. Int J Cancer. 2014.
102. Yu T, Li J, Yan M, Liu L, Lin H, Zhao F, Sun L, Zhang Y, Cui Y, Zhang F. 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. 2014; 1351:531-542.
103. Cimino D, De Pittà C, Orso F, Zampini M, Casara S, Penna E, Quaglino E, Forni M, Damasco C, Pinatel E. miR148b is a major coordinator of breast cancer progression in a relapse-associated microRNA signature by targeting ITGA5, ROCK1, PIK3CA, NRAS, and CSF1. The FASEB Journal. 2013; 27:1223-1235.
104. Liao WT, Ye YP, Zhang NJ, Li TT, Wang SY, Cui YM, Qi L, Wu P, Jiao HL, Xie YJ. MicroRNA-30b functions as a tumour suppressor in human colorectal cancer by targeting KRAS, PIK3CD and BCL2. The Journal of pathology. 2014; 232:415-427.
105. Shi Y, Chen C, Zhang X, Liu Q, Xu J-L, Zhang H-R, Yao X-H, Jiang T, He Z-C, Ren Y. Primate-specific miR-663 functions as a tumor suppressor by targeting PIK3CD and predicts the prognosis of human glioblastoma. Clin Cancer Res. 2014; 20:1803-1813.
106. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 2007; 133:647-658.
107. Yang H, Kong W, He L, Zhao J-J, O'Donnell JD, Wang J, Wenham RM, Coppola D, Kruk PA, Nicosia SV. MicroRNA expression profiling in human ovarian cancer:miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 2008; 68:425-433.
108. Kato M, Putta S, Wang M, Yuan H, Lanting L, Nair I, Gunn A, Nakagawa Y, Shimano H, Todorov I. TGF-β activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol. 2009; 11:881-889.
109. Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, Sohn-Lee C, le Sage C, Agami R, Tuschl T. The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev. 2009; 23:1327-1337.
110. Mouw JK, Yui Y, Damiano L, Bainer RO, Lakins JN, Acerbi I, Ou G, Wijekoon AC, Levental KR, Gilbert PM. Tissue mechanics modulate microRNAdependent PTEN expression to regulate malignant progression. Nat Med. 2014; 20:360-367.
111. Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T, Hijiya N, Matsuura K, Fujioka T, Seto M. MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3ζ. Cancer Res. 2010; 70:2339-2349.
112. Yoo J, Jung H, Lee J, Yi H, Oh S, Ko H, Yoo H, Kim H, Song H, Kim S. The novel miR-9500 regulates the proliferation and migration of human lung cancer cells by targeting Akt1. Cell Death & Differentiation. 2014.
113. Cai N, Wang Y-D, Zheng P-S. The microRNA-302-367 cluster suppresses the proliferation of cervical carcinoma cells through the novel target AKT1. RNA. 2013; 19:85-95.
114. Wang J, Yang K, Zhou L, Wu Y, Zhu M, Lai X, Chen T, Feng L, Li M, Huang C. MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Path. 2013; 9:e1003697.
115. Yang K, Wu M, Li M, Li D, Peng A, Nie X, Sun M, Wang J, Wu Y, Deng Q. miR-155 suppresses bacterial clearance in Pseudomonas aeruginosa keratitis by targeting Rheb. J Infect Dis. 2014; 210:89-98.
116. Deng M, Tang H, Zhou Y, Zhou M, Xiong W, Zheng Y, Ye Q, Zeng X, Liao Q, Guo X. miR-216b suppresses tumor growth and invasion by targeting KRAS in nasopharyngeal carcinoma. J Cell Sci. 2011; 124:2997-3005.
117. Hatley ME, Patrick DM, Garcia MR, Richardson JA, Bassel-Duby R, Van Rooij E, Olson EN. Modulation of K-Ras-dependent lung tumorigenesis by MicroRNA-21. Cancer Cell. 2010; 18:282-293.
118. Yang G, Wu D, Zhu J, Jiang O, Shi Q, Tian J, Weng Y. Upregulation of miR-195 increases the sensitivity of breast cancer cells to Adriamycin treatment through inhibition of Raf-1. Oncol Rep. 2013; 30:877-889.
119. Hirata H, Hinoda Y, Ueno K, Shahryari V, Tabatabai ZL, Dahiya R. MicroRNA-1826 targets VEGFC, beta-catenin (CTNNB1) and MEK1 (MAP2K1) in human bladder cancer. Carcinogenesis. 2012; 33:41-48.
120. Ichimura A, Ruike Y, Terasawa K, Shimizu K, Tsujimoto G. miR-34a inhibits cell proliferation by repressing MEK1 during megakaryocytic differentiation of K562. Mol Pharmacol. 2010; . mol. 109.063321.
121. Wang L, Shi M, Hou S, Ding B, Liu L, Ji X, Zhang J, Deng Y. MiR-483-5p suppresses the proliferation of glioma cells via directly targeting ERK1. FEBS Lett. 2012; 586:1312-1317.
122. Wang F, Xiong L, Huang X, Zhao T, Wu L-y, Liu Z-h, Ding X, Liu S, Wu Y, Zhao Y. miR-210 suppresses BNIP3 to protect against the apoptosis of neural progenitor cells. Stem cell research. 2013; 11:657-667.
123. Hwang-Verslues W, Chang P, Wei P, Yang C, Huang C, Kuo W, Shew J, Chang K, Lee EYP, Lee W. miR-495 is upregulated by E12/E47 in breast cancer stem cells, and promotes oncogenesis and hypoxia resistance via downregulation of E-cadherin and REDD1. Oncogene. 2011; 30:2463-2474.
124. Chan FK-M. Programmed Necrosis/Necroptosis: An Inflammatory Form of Cell Death. Cell Death. Springer 2014; :211-228.
125. Zhou W, Yuan J. SnapShot: Necroptosis. Cell. 2014; 158:464-464. e461.
126. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol. 2005; 1:112-119.
127. Zhou W, Yuan J. Necroptosis in health and diseases. Semin Cell Dev Biol. Elsevier 2014; 35:14-23.
128. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell. 2009; 137:1100-1111.
129. Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012; 148:213-227.
130. Cai Z, Jitkaew S, Zhao J, Chiang H-C, Choksi S, Liu J, Ward Y, Wu L-g, Liu Z-G. Plasma membrane translocation of trimerized MLKL protein is required for TNFinduced necroptosis. Nat Cell Biol. 2014; 16:55-65.
131. Wang Z, Jiang H, Chen S, Du F, Wang X. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell. 2012; 148:228-243.
132. Liu J, van Mil A, Vrijsen K, Zhao J, Gao L, Metz CH, Goumans MJ, Doevendans PA, Sluijter JP. MicroRNA-5 prevents necrotic cell death in human cardiomyocyte progenitor cells via targeting RIP1. J Cell Mol Med. 2011; 15:1474-1482.
133. Wang J-X, Jiao J-Q, Li Q, Long B, Wang K, Liu J-P, Li Y-R, Li P-F. miR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat Med. 2011; 17:71-78.
134. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell. 2010; 39:493-506.
135. Ye H, Liu X, Lv M, Wu Y, Kuang S, Gong J, Yuan P, Zhong Z, Li Q, Jia H. MicroRNA and transcription factor co-regulatory network analysis reveals miR-19 inhibits CYLD in T-cell acute lymphoblastic leukemia. Nucleic Acids Res. 2012; 40:5201-5214.
136. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005; 122:927-939.
137. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1- mediated phosphorylation of Bcl-2 regulates starvationinduced autophagy. Mol Cell. 2008; 30:678-688.
138. Zalckvar E, Berissi H, Mizrachy L, Idelchuk Y, Koren I, Eisenstein M, Sabanay H, Pinkas-Kramarski R, Kimchi A. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO reports. 2009; 10:285-292.
139. Wirawan E, Walle LV, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I, Roelandt R, De Rycke R, Verspurten J, Declercq W. Caspase-mediated cleavage of Beclin- inactivates Beclin-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death & Disease. 2010; 1:e18.
140. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon H-U. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol. 2006; 8:1124-1132.
141. Bhutia SK, Dash R, Das SK, Azab B, Su Z-z, Lee S-G, Grant S, Yacoub A, Dent P, Curiel DT. Mechanism of autophagy to apoptosis switch triggered in prostate cancer cells by antitumor cytokine melanoma differentiation- associated gene 7/interleukin-24. Cancer Res. 2010; 70:3667-3676.
142. Moscat J, Diaz-Meco MT. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell. 2009; 137:1001-1004.
143. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell. 2006; 126:121-134.
144. Lee J-S, Li Q, Lee J-Y, Lee S-H, Jeong JH, Lee H-R, Chang H, Zhou F-C, Gao S-J, Liang C. FLIP-mediated autophagy regulation in cell death control. Nat Cell Biol. 2009; 11:1355-1362.
145. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C, Hakem R, Salvesen GS, Green DR. Catalytic activity of the caspase-8-FLIPL complex inhibits RIPK3-dependent necrosis. Nature. 2011; 471:363-367.
146. Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C, Hupe M, Cain K, MacFarlane M, Häcker G, Leverkus M. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell. 2011; 43:449-463.