Interaction of autophagy with microRNAs and their potential therapeutic implications in human cancers

Cancer Letters

Volumn 356, Issue 2, 2015, Pages 332-338

  Jing, Zhao ^a   Han, Weidong ^a   Sui, Xinbing ^a   Xie, Jiansheng ^a   Pan, Hongming ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Antagomirs; Autophagy; Cancer; MiRNAs

Indexed keywords

BECLIN 1; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; LIPOSOME; MICRORNA; MICRORNA 26A; MICRORNA 30A; MICRORNA 34A; PARVOVIRUS VECTOR; PROTEIN BCL 2; PROTEIN P62; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT;

3' UNTRANSLATED REGION; AUTOPHAGY; BINDING AFFINITY; BIOGENESIS; BREAST CANCER; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL DEATH; CELL INTERACTION; DOWN REGULATION; GENE DELIVERY SYSTEM; GENE EXPRESSION REGULATION; GENE TARGETING; HEAD AND NECK CARCINOMA; HOMEOSTASIS; HUMAN; LIVER CANCER; LUNG CANCER; MEDICAL LITERATURE; MOLECULAR DYNAMICS; MYOBLAST; NEOPLASM; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA SYNTHESIS; RNA TRANSCRIPTION; SHORT SURVEY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; DISEASE COURSE; DRUG EFFECTS; GENETICS; NEOPLASMS;

EUKARYOTA;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84919430038     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.09.039     Document Type: Review

References (92)

1. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
2. Levine B., Kroemer G. Autophagy in aging, disease and death: the true identity of a cell death impostor. Cell Death Differ 2009, 16:1-2.
3. Yang Z., Klionsky D.J. Eaten alive: a history of macroautophagy. Nat. Cell Biol 2010, 12:814-822.
4. Cuervo A.M., Wong E. Chaperone-mediated autophagy: roles in disease and aging. Cell Res 2014, 24:92-104.
5. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
6. Kroemer G., Marino G., Levine B. Autophagy and the integrated stress response. Mol. Cell 2010, 40:280-293.
7. Clarke P.G., Puyal J. Autophagic cell death exists. Autophagy 2012, 8:867-869.
8. Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012, 19:107-120.
9. Loos B., Engelbrecht A.M., Lockshin R.A., Klionsky D.J., Zakeri Z. The variability of autophagy and cell death susceptibility: unanswered questions. Autophagy 2013, 9:1270-1285.
10. Zhou S., Zhao L., Kuang M., Zhang B., Liang Z., Yi T., et al. Autophagy in tumorigenesis and cancer therapy: Dr. Jekyll or Mr. Hyde?. Cancer Lett 2012, 323:115-127.
11. Lavandero S., Troncoso R., Rothermel B.A., Martinet W., Sadoshima J., Hill J.A. Cardiovascular autophagy: concepts, controversies, and perspectives. Autophagy 2013, 9:1455-1466.
12. He C., Klionsky D.J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet 2009, 43:67-93.
13. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
14. Stahlhut C., Slack F.J. MicroRNAs and the cancer phenotype: profiling, signatures and clinical implications. Genome Med 2013, 5:111.
15. Serpico D., Molino L., Di Cosimo S. microRNAs in breast cancer development and treatment. Cancer Treat. Rev 2014, 40:595-604.
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, 5:816-823.
17. Ganley I.G., du Lam H., Wang J., Ding X., Chen S., Jiang X. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem 2009, 284:12297-12305.
18. Hosokawa N., Sasaki T., Iemura S., Natsume T., Hara T., Mizushima N. Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 2009, 5:973-979.
19. Chen Y., Liersch R., Detmar M. The miR-290-295 cluster suppresses autophagic cell death of melanoma cells. Sci. Rep 2012, 2:808.
20. Wu H., Wang F., Hu S., Yin C., Li X., Zhao S., et al. 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.
21. Wang Z., Wang N., Liu P., Chen Q., Situ H., Xie T., et al. MicroRNA-25 regulates chemoresistance-associated autophagy in breast cancer cells, a process modulated by the natural autophagy inducer isoliquiritigenin. Oncotarget 2014, 5:7013-7026.
22. Huang Y., Chuang A.Y., Ratovitski E.A. Phospho-DeltaNp63alpha/miR-885-3p axis in tumor cell life and cell death upon cisplatin exposure. Cell Cycle 2011, 10:3938-3947.
23. Tang B., Li N., Gu J., Zhuang Y., Li Q., Wang H.G., et al. Compromised autophagy by MIR30B benefits the intracellular survival of Helicobacter pylori. Autophagy 2012, 8:1045-1057.
24. Korkmaz G., le Sage C., Tekirdag K.A., Agami R., Gozuacik D. miR-376b controls starvation and mTOR inhibition-related autophagy by targeting ATG4C and BECN1. Autophagy 2012, 8:165-176.
25. Menghini R., Casagrande V., Marino A., Marchetti V., Cardellini M., Stoehr R., et al. MiR-216a: a link between endothelial dysfunction and autophagy. Cell Death Dis 2014, 5:e1029.
26. Chatterjee A., Chattopadhyay D., Chakrabarti G. miR-17-5p downregulation contributes to paclitaxel resistance of lung cancer cells through altering beclin1 expression. PLoS ONE 2014, 9:e95716.
27. Huang Y., Guerrero-Preston R., Ratovitski E.A. Phospho-DeltaNp63alpha-dependent regulation of autophagic signaling through transcription and micro-RNA modulation. Cell Cycle 2012, 11:1247-1259.
28. Shi G., Shi J., Liu K., Liu N., Wang Y., Fu Z., et al. Increased miR-195 aggravates neuropathic pain by inhibiting autophagy following peripheral nerve injury. Glia 2013, 61:504-512.
29. Frankel L.B., Wen J., Lees M., Hoyer-Hansen M., Farkas T., Krogh A., et al. microRNA-101 is a potent inhibitor of autophagy. EMBO J. 2011, 30:4628-4641.
30. Ravikumar B., Imarisio S., Sarkar S., O'Kane C.J., Rubinsztein D.C. Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J. Cell Sci 2008, 121:1649-1660.
31. Korkmaz G., Tekirdag K.A., Ozturk D.G., Kosar A., Sezerman O.U., Gozuacik D. MIR376A is a regulator of starvation-induced autophagy. PLoS ONE 2013, 8:e82556.
32. Chang Y., Yan W., He X., Zhang L., Li C., Huang H., et al. miR-375 inhibits autophagy and reduces viability of hepatocellular carcinoma cells under hypoxic conditions. Gastroenterology 2012, 143:177-187.
33. Comincini S., Allavena G., Palumbo S., Morini M., Durando F., Angeletti F., et al. microRNA-17 regulates the expression of ATG7 and modulates the autophagy process, improving the sensitivity to temozolomide and low-dose ionizing radiation treatments in human glioblastoma cells. Cancer Biol. Ther 2013, 14:574-586.
34. Mikhaylova O., Stratton Y., Hall D., Kellner E., Ehmer B., Drew A.F., et al. VHL-regulated MiR-204 suppresses tumor growth through inhibition of LC3B-mediated autophagy in renal clear cell carcinoma. Cancer Cell 2012, 21:532-546.
35. Lu C., Chen J., Xu H.G., Zhou X., He Q., Li Y.L., et al. MIR106B and MIR93 prevent removal of bacteria from epithelial cells by disrupting ATG16L1-mediated autophagy. Gastroenterology 2014, 146:188-199.
36. Zhai Z., Wu F., Dong F., Chuang A.Y., Messer J.S., Boone D.L., et al. Human autophagy gene ATG16L1 is post-transcriptionally regulated by MIR142-3p. Autophagy 2014, 10:468-479.
37. Nguyen H.T., Dalmasso G., Muller S., Carriere J., Seibold F., Darfeuille-Michaud A. Crohn's disease-associated adherent invasive Escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology 2014, 146:508-519.
38. Tekirdag K.A., Korkmaz G., Ozturk D.G., Agami R., Gozuacik D. MIR181A regulates starvation- and rapamycin-induced autophagy through targeting of ATG5. Autophagy 2013, 9:374-385.
39. Kovaleva V., Mora R., Park Y.J., Plass C., Chiramel A.I., Bartenschlager R., et al. miRNA-130a targets ATG2B and DICER1 to inhibit autophagy and trigger killing of chronic lymphocytic leukemia cells. Cancer Res 2012, 72:1763-1772.
40. Yang J., Chen D., He Y., Melendez A., Feng Z., Hong Q., et al. MiR-34 modulates Caenorhabditis elegans lifespan via repressing the autophagy gene atg9. Age (Dordr) 2013, 35:11-22.
41. Jegga A.G., Schneider L., Ouyang X., Zhang J. Systems biology of the autophagy-lysosomal pathway. Autophagy 2011, 7:477-489.
42. Bo L., Su-Ling D., Fang L., Lu-Yu Z., Tao A., Stefan D., et al. Autophagic program is regulated by miR-325. Cell Death Differ 2014, 21:967-977.
43. Singh S.B., 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, 12:1154-1165.
44. 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, 43:242-245.
45. Roccaro A.M., Sacco A., Jia X., Azab A.K., Maiso P., Ngo H.T., et al. microRNA-dependent modulation of histone acetylation in Waldenstrom macroglobulinemia. Blood 2010, 116:1506-1514.
46. Yan D., Dong X.D., Chen X., Yao S., Wang L., Wang J., et al. Role of microRNA-182 in posterior uveal melanoma: regulation of tumor development through MITF, BCL2 and cyclin D2. PLoS ONE 2012, 7:e40967.
47. Li L., Yuan L., Luo J., Gao J., Guo J., Xie X. MiR-34a inhibits proliferation and migration of breast cancer through down-regulation of Bcl-2 and SIRT1. Clin. Exp. Med 2013, 13:109-117.
48. Chio C.C., Lin J.W., Cheng H.A., Chiu W.T., Wang Y.H., Wang J.J., et al. MicroRNA-210 targets antiapoptotic Bcl-2 expression and mediates hypoxia-induced apoptosis of neuroblastoma cells. Arch. Toxicol 2013, 87:459-468.
49. Tian L., Zhang J., Ge J., Xiao H., Lu J., Fu S., et al. MicroRNA-205 suppresses proliferation and promotes apoptosis in laryngeal squamous cell carcinoma. Med. Oncol 2014, 31:785.
50. Wu Z., Lu H., Sheng J., Li L. Inductive microRNA-21 impairs anti-mycobacterial responses by targeting IL-12 and Bcl-2. FEBS Lett 2012, 586:2459-2467.
51. Meenhuis A., van Veelen P.A., de Looper H., van Boxtel N., van den Berge I.J., Sun S.M., et al. MiR-17/20/93/106 promote hematopoietic cell expansion by targeting sequestosome 1-regulated pathways in mice. Blood 2011, 118:916-925.
52. Wan G., Xie W., Liu Z., Xu W., Lao Y., Huang N., et al. Hypoxia-induced MIR155 is a potent autophagy inducer by targeting multiple players in the MTOR pathway. Autophagy 2014, 10:70-79.
53. Ge Y.Y., Shi Q., Zheng Z.Y., Gong J., Zeng C., Yang J., et al. MicroRNA-100 promotes the autophagy of hepatocellular carcinoma cells by inhibiting the expression of mTOR and IGF-1R. Oncotarget 2014, 5:6218-6228.
54. Pan B., Yi J., Song H. MicroRNA-mediated autophagic signaling networks and cancer chemoresistance. Cancer Biother. Radiopharm 2013, 28:573-578.
55. Yu Y., Yang L., Zhao M., Zhu S., Kang R., Vernon P., et al. Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronic myeloid leukemia cells. Leukemia 2012, 26:1752-1760.
56. Wang P., Zhang J., Zhang L., Zhu Z., Fan J., Chen L., et al. MicroRNA 23b regulates autophagy associated with radioresistance of pancreatic cancer cells. Gastroenterology 2013, 145:1133-1143.
57. Gibbings D., Mostowy S., Jay F., Schwab Y., Cossart P., Voinnet O. Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nat. Cell Biol 2012, 14:1314-1321.
58. Zhang P., Zhang H. Autophagy modulates miRNA-mediated gene silencing and selectively degrades AIN-1/GW182 in C. elegans. EMBO Rep 2013, 14:568-576.
59. Lan S.H., Wu S.Y., Zuchini R., Lin X.Z., Su I.J., Tsai T.F., et al. Autophagy suppresses tumorigenesis of hepatitis B virus-associated hepatocellular carcinoma through degradation of microRNA-224. Hepatology 2014, 59:505-517.
60. Guo J.Y., Xia B., White E. Autophagy-mediated tumor promotion. Cell 2013, 155:1216-1219.
61. Rao S., Tortola L., Perlot T., Wirnsberger G., Novatchkova M., Nitsch R., et al. A dual role for autophagy in a murine model of lung cancer. Nat. Commun 2014, 5:3056.
62. Jiang P., Mizushima N. Autophagy and human diseases. Cell Res 2014, 24:69-79.
63. Maes H., Rubio N., Garg A.D., Agostinis P. Autophagy: shaping the tumor microenvironment and therapeutic response. Trends Mol. Med 2013, 19:428-446.
64. Zhai H., Song B., Xu X., Zhu W., Ju J. Inhibition of autophagy and tumor growth in colon cancer by miR-502. Oncogene 2013, 32:1570-1579.
65. Xu L., Beckebaum S., Iacob S., Wu G., Kaiser G.M., Radtke A., et al. MicroRNA-101 inhibits human hepatocellular carcinoma progression through EZH2 downregulation and increased cytostatic drug sensitivity. J. Hepatol 2014, 60:590-598.
66. Xu Y., An Y., Wang Y., Zhang C., Zhang H., Huang C., et al. miR-101 inhibits autophagy and enhances cisplatin-induced apoptosis in hepatocellular carcinoma cells. Oncol. Rep 2013, 29:2019-2024.
67. Zou Z., Wu L., Ding H., Wang Y., Zhang Y., Chen X., et al. MicroRNA-30a sensitizes tumor cells to cis-platinum via suppressing beclin 1-mediated autophagy. J. Biol. Chem 2012, 287:4148-4156.
68. Zhang Y., Yang W.Q., Zhu H., Qian Y.Y., Zhou L., Ren Y.J., et al. Regulation of autophagy by miR-30d impacts sensitivity of anaplastic thyroid carcinoma to cisplatin. Biochem. Pharmacol 2014, 87:562-570.
69. Pennati M., Lopergolo A., Profumo V., De Cesare M., Sbarra S., Valdagni R., et al. miR-205 impairs the autophagic flux and enhances cisplatin cytotoxicity in castration-resistant prostate cancer cells. Biochem. Pharmacol 2014, 87:579-597.
70. Wang Z., Ting Z., Li Y., Chen G., Lu Y., Hao X. microRNA-199a is able to reverse cisplatin resistance in human ovarian cancer cells through the inhibition of mammalian target of rapamycin. Oncol. Lett 2013, 6:789-794.
71. Gwak H.S., Kim T.H., Jo G.H., Kim Y.J., Kwak H.J., Kim J.H., et al. Silencing of microRNA-21 confers radio-sensitivity through inhibition of the PI3K/AKT pathway and enhancing autophagy in malignant glioma cell lines. PLoS ONE 2012, 7:e47449.
72. Seca H., Lima R.T., Lopes-Rodrigues V., Guimaraes J.E., Almeida G.M., Vasconcelos M.H. Targeting miR-21 induces autophagy and chemosensitivity of leukemia cells. Curr. Drug Targets 2013, 14:1135-1143.
73. Shum D., Bhinder B., Radu C., Farazi T., Landthaler M., Tuschl T., et al. An image-based biosensor assay strategy to screen for modulators of the microRNA 21 biogenesis pathway. Comb. Chem. High Throughput Screen 2012, 15:529-541.
74. Bose D., Jayaraj G.G., Kumar S., Maiti S. A molecular-beacon-based screen for small molecule inhibitors of miRNA maturation. ACS Chem. Biol 2013, 8:930-938.
75. Shibuta T., Honda E., Shiotsu H., Tanaka Y., Vellasamy S., Shiratsuchi M., et al. Imatinib induces demethylation of miR-203 gene: an epigenetic mechanism of anti-tumor effect of imatinib. Leuk. Res 2013, 37:1278-1286.
76. Jian P., Li Z.W., Fang T.Y., Jian W., Zhuan Z., Mei L.X., et al. Retinoic acid induces HL-60 cell differentiation via the upregulation of miR-663. J. Hematol. Oncol 2011, 4:20.
77. Stenvang J., Petri A., Lindow M., Obad S., Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence 2012, 3:1.
78. Broderick J.A., Zamore P.D. MicroRNA therapeutics. Gene Ther 2011, 18:1104-1110.
79. Lanford R.E., Hildebrandt-Eriksen E.S., Petri A., Persson R., Lindow M., Munk M.E., et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010, 327:198-201.
80. Murphy B.L., Obad S., Bihannic L., Ayrault O., Zindy F., Kauppinen S., et al. Silencing of the miR-17~92 cluster family inhibits medulloblastoma progression. Cancer Res 2013, 73:7068-7078.
81. Bader A.G., Brown D., Stoudemire J., Lammers P. Developing therapeutic microRNAs for cancer. Gene Ther 2011, 18:1121-1126.
82. Wang Q.Z., Lv Y.H., Gong Y.H., Li Z.F., Xu W., Diao Y., et al. Double-stranded Let-7 mimics, potential candidates for cancer gene therapy. J. Physiol. Biochem 2012, 68:107-119.
83. Di Martino M.T., Leone E., Amodio N., Foresta U., Lionetti M., Pitari M.R., et al. Synthetic miR-34a mimics as a novel therapeutic agent for multiple myeloma: in vitro and in vivo evidence. Clin. Cancer Res 2012, 18:6260-6270.
84. Pacak C.A., Byrne B.J. AAV vectors for cardiac gene transfer: experimental tools and clinical opportunities. Mol. Ther 2011, 19:1582-1590.
85. Kota J., Chivukula R.R., O'Donnell K.A., Wentzel E.A., Montgomery C.L., Hwang H.W., et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009, 137:1005-1017.
86. Miller A.D. Delivery of RNAi therapeutics: work in progress. Expert Rev. Med. Devices 2013, 10:781-811.
87. Trang P., Wiggins J.F., Daige C.L., Cho C., Omotola M., Brown D., et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol. Ther 2011, 19:1116-1122.
88. Piao L., Zhang M., Datta J., Xie X., Su T., Li H., et al. Lipid-based nanoparticle delivery of Pre-miR-107 inhibits the tumorigenicity of head and neck squamous cell carcinoma. Mol. Ther 2012, 20:1261-1269.
89. Li L., Xie X., Luo J., Liu M., Xi S., Guo J., et al. Targeted expression of miR-34a using the T-VISA system suppresses breast cancer cell growth and invasion. Mol. Ther 2012, 20:2326-2334.
90. Liang G.F., Zhu Y.L., Sun B., Hu F.H., Tian T., Li S.C., et al. PLGA-based gene delivering nanoparticle enhance suppression effect of miRNA in HePG2 cells. Nanoscale Res Lett 2011, 6:447.
91. Cao M., Deng X., Su S., Zhang F., Xiao X., Hu Q., et al. Protamine sulfate-nanodiamond hybrid nanoparticles as a vector for MiR-203 restoration in esophageal carcinoma cells. Nanoscale 2013, 5:12120-12125.
92. Griveau A., Bejaud J., Anthiya S., Avril S., Autret D., Garcion E. Silencing of miR-21 by locked nucleic acid-lipid nanocapsule complexes sensitize human glioblastoma cells to radiation-induced cell death. Int. J. Pharm 2013, 454:765-774.