MicroRNA-34a: A potential therapeutic target in human cancer

Cell Death and Disease

Volumn 5, Issue 7, 2014, Pages

  Li, X J ^a   Ren, R J ^a   Tang, J H ^a  

^a JIANGSU CANCER HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA 34A; MICRORNA; MIRN34 MICRORNA, HUMAN;

APOPTOSIS; BLADDER CANCER; BRAIN TUMOR; BREAST CANCER; CANCER THERAPY; CARCINOGENESIS; CELL PROLIFERATION; CLINICAL TRIAL; COLON CANCER; DEREGULATION; DRUG TARGETING; EWING SARCOMA; GENE EXPRESSION; HUMAN; LEUKEMIA; LIVER CELL CARCINOMA; LUNG CANCER; MELANOMA; MYELOMA; NEUROBLASTOMA; NONHUMAN; ONCOGENE; OSTEOSARCOMA; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; REVIEW; TUMOR INVASION; TUMOR SUPPRESSOR GENE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASMS;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; MICRORNAS; NEOPLASMS;

EID: 84905499878     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.270     Document Type: Review

References (95)

1. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell 2009; 136: 215-233
2. Meijer HA, Kong YW, Lu WT, Wilczynska A, Spriggs RV, Robinson SW et al. Translational repression and eIF4A2 activity are critical for microRNA-Mediated gene regulation. Science 2013; 340: 82-85
3. Eiring AM, Harb JG, Neviani P, Garton C, Oaks JJ, Spizzo R et al. miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 2010; 140: 652-665
4. Kim DH, Saetrom P, Snove Jr O, Rossi JJ. MicroRNA-Directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci USA 2008; 105: 16230-16235
5. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447: 1130-1134
6. Adachi N, Lieber MR. Bidirectional gene organization: A common architectural feature of the human genome. Cell 2002; 109: 807-809
7. Buanne P, Corrente G, Micheli L. Cloning of PC3B, a novel member of the PC3/BTG/TOB family of growth inhibitory genes, highly expressed in the olfactory epithelium. Genomics 2000; 68: 253-263
8. Nagai H, Negrini M, Carter SL, Gillum DR, Rosenberg AL. Detection and cloning of a common region of loss of heterozygosity at chromosome 1p in breast cancer. Cancer Res 1995; 55: 1752-1757
9. Attiyeh EF, London WB, Mossé YP, Wang Q, Winter C, Khazi D et al. Children's oncology Group. Chromosome 1p and 11q deletions and outcome in neuroblastoma. N Engl J Med 2005; 24: 2243-2253
10. Zhang H, Zhai Y, Hu Z, Wu C, Qian J, JiaWet al. Genome-Wide association study identifies 1p36.22 as a new susceptibility locus for hepatocellular carcinoma in chronic hepatitis B virus carriers. Nat Genet 2010; 42: 755-758
11. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Körner H et al. Inactivation of miR34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008; 7: 2591-2600
12. Baer C, Claus R, Frenzel LP, Zucknick M, Park YJ, Gu L et al. Extensive promoter DNA hypermethylation and hypomethylation is associated with aberrant microRNA expression in chronic lymphocytic leukemia. Cancer Res 2012; 72: 3775-3785
13. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE et al. p53-Mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007; 17: 1298-1307
14. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH et al. Transactivation of miR34a by p53 broadly influences gene expression and promotes apop-Tosis. Mol Cell 2007; 26: 745-752
15. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N et al. Transcriptional activation of miR34a contributes to p53-Mediated apoptosis. Mol Cell 2007; 26: 731-743
16. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A et al. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007; 6: 1586-1593
17. Yamakuchi M, MiR-34 Lowenstein CJ. SIRT1 and p53: The feedback loop. Cell Cycle 2009; 8: 712-715
18. Yamakuchi M, Ferlito M, Lowenstein CJ. miR34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA 2008; 105: 13421-13426
19. Mandke P, Wyatt N, Fraser J, Bates B, Berberich SJ, Markey MP. MicroRNA-34a modulates MDM4 expression via a target site in the open reading frame. PLoS One 2012; 7: e42034
20. Weeraratne SD, Amani V, Neiss A, Teider N, Scott DK. miR34a confers chemosensitivity through modulation of MAGE-A and p53 in medulloblastoma. Neuro Oncol 2010; 13: 165-175
21. Chen QR, Yu LR, Tsang P, Wei JS, Song YK. Systematic proteome analysis identifies transcription factor YY1 as a direct target of miR34a. J Proteome Res 2011; 10: 479-487
22. Sui G, Affar el B, Shi Y, Brignone C, Wall NR, Yin P et al. Yin Yang 1 is a negative regulator of p53. Cell 2004; 117: 859-872
23. Christoffersen NR, Shalgi R, Frankel LB, Leucci E. p53-independent upregulation of miR34a during oncogene-induced senescence represses MYC. Cell Death Differ 2010; 17: 236-245
24. Baer C, Claus R, Plass C. Genome-Wide epigenetic regulation of miRNAs in cancer. Cancer Res 2013; 73: 473-477
25. Agostini M, Tucci P, Killick R, Candi E, Sayan BS, Rivetti di Val Cervo P et al. Neuronal differentiation by TAp73 is mediated by microRNA-34a regulation of synaptic protein targets. Proc Natl Acad Sci USA 2011; 108: 21093-21098
26. Antonini D, Russo MT, De Rosa L, Gorrese M, Del Vecchio L, Missero C. Transcriptional repression of MiR-34 family contributes to p63-Mediated cell cycle progression in epidermal cells. J Invest Dermatol 2010; 130: 1249-1257
27. Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, Götz U et al. MiR-34 and SNAIL form a double-Negative feedback loop to regulate epithelial-Mesenchymal transitions. Cell Cycle 2011; 10: 4256-4271
28. Wouters BG, Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 2008; 8: 851-864
29. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H. A microRNA signature of hypoxia. Mol Cell Biol 2007; 27: 1859-1867
30. Du R, Sun WJ, Xia L, Zhao A, Yu Y, Zhao LJ et al. Hypoxia-induced down-Regulation of microRNA-34a promotes EMT by targeting the Notch signaling pathway in tubular epithelial cells. PLoS One 2012; 7: e30771
31. Lu X, Chen Z, Liang H, Li Z, Zou X, Luo H et al. Thyroid hormone inhibits TGFb1 induced renal tubular epithelial to mesenchymal transition by increasing miR34a expression. Cell Signal 2013; 25: 1949-1954
32. Zhao G, Guo J, Li D, Jia C, Yin W, Sun R et al. MicroRNA-34a suppresses cell proliferation by targeting LMTK3 in human breast cancer mcf-7 cell line. DNA Cell Biol 2013; 32: 699-707
33. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG et al. Epigenetic inactivation of the miR34a in hematological malignancies. Carcinogenesis 2010; 31: 745-750
34. Bagchi A, Mills AA. The quest for the 1p36 tumor suppressor. Cancer Res 2008; 68: 2551-2556
35. Welch C, Chen Y, Stallings RL. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 2007; 26: 5017-5022
36. Cole KA, Attiyeh EF, Mosse YP, Laquaglia MJ, Diskin SJ, Brodeur GM et al. A functional screen identifies miR34a as a candidate neuroblastoma tumor suppressor gene. Mol Cancer Res 2008; 6: 735-742
37. Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y et al. miR34a inhibits migration and invasion by down-Regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 2009; 275: 44-53
38. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L et al. MicroRNA MiR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009; 4: e6816
39. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 2009; 69: 7569-7576
40. Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D et al. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 2010; 70: 5923-5930
41. Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-Suppressive miR34a induces senescence-Like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci USA 2007; 104: 15472-15477
42. Kato M, Paranjape T, Ullrich R, Nallur S, Gillespie E, Keane K et al. The MiR-34 microRNA is required for the DNA damage response in vivo in C. elegans and in vitro in human breast cancer cells. Oncogene 2009; 28: 2419-2424
43. Pang RT, Leung CO, Ye TM, Liu W, Chiu PC, Lam KK et al. MicroRNA-34a suppresses invasion through downregulation of Notch1 and Jagged1 in cervical carcinoma and choriocarcinoma cells. Carcinogenesis 2010; 31: 1037-1044
44. Concepcion CP, Han YC, Mu P, Bonetti C, Yao E, D'Andrea A et al. Intact p53-Dependent responses in miR-34-Deficient mice. PLoS Genet 2012; 8: e1002797
45. Bieche I, Khodja A, Lidereau R. Deletion mapping of chromosomal region 1p32-Pter in primary breast cancer. Genes Chromosomes Cancer 1999; 24: 255-263
46. Nagai H, Negrini M, Carter SL, Gillum DR, Rosenberg AL, Schwartz GF et al. Detection and cloning of a common region of loss of heterozygosity at chromosome 1p in breast cancer. Cancer Res 1995; 55: 1752-1757
47. Yang S, Li Y, Gao J, Zhang T, Li S, Luo A et al. MicroRNA-34 suppresses breast cancer invasion and metastasis by directly targeting Fra-1. Oncogene 2012; 24: 432
48. Li XJ, Ji MH, Zhong SL, Zha QB, Xu JJ, Zhao JH et al. MicroRNA-34a modulates chemosensitivity of breast cancer cells to adriamycin by targeting. Notch1. Arch Med Res 2012; 43: 514-521
49. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: Cell fate control and signal integration in development. Science 1999; 284: 770-776
50. Chen GQ, Zhao ZW, Zhou HY, Liu YJ, Yang HJ. Systematic analysis of microRNA involved in resistance of the MCF-7 human breast cancer cell to doxorubicin. Med Oncol 2010; 27: 406-415
51. Kastl L, Brown I, Schofield AC. miRNA-34a is associated with docetaxel resistance in human breast cancer cells. Breast Cancer Res Treat 2012; 131: 445-454
52. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105: 10513-10518
53. Roth C, Rack B, Müller V, Janni W, Pantel K, Schwarzenbach H. Circulating microRNAs as blood-Based markers for patients with primary and metastatic breast cancer. Breast Cancer Res 2010; 12: 54
54. Eichelser C, Flesch-Janys D, Chang-Claude J, Pantel K, Schwarzenbach H. Deregulated serum concentrations of circulating cell-Free microRNAs miR-17, miR34a, miR-155, and miR-373 in human breast cancer development and progression. Clin Chem 2013; 59: 1489-1496
55. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T et al. Cancer statistics. CA Cancer J Clin 2008; 58: 71-96
56. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435: 834-838
57. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F et al. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 2008; 68: 6162-6170
58. Ozen M, Creighton CJ, Ozdemir M, Ittmann M. Widespread deregulation of microRNA expression in human prostate cancer. Oncogene 2008; 27: 1788-1793
59. 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 USA 2006; 103: 2257-2261
60. Antonov AV, Knight RA, Melino G, Barlev NA, Tsvetkov PO. MIRUMIR: An online tool to test microRNAs as biomarkers to predict survival in cancer using multiple clinical data sets. Cell Death Differ 2013; 20: 367
61. Yamamura S, Saini S, Majid S, Hirata H, Ueno K, Deng G et al. MicroRNA-34a modulates c-Myc transcriptional complexes to suppress malignancy in human prostate cancer cells. PLoS One 2012; 7: e29722
62. Croce CM, Calin GA. miRNAs, cancer, and stem cell division. Cell 2005; 122: 6-7
63. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T. The microRNA miR34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 2011; 17: 211-215
64. Cheng CY, Hwang CI, Corney DC, Flesken-Nikitin A, Jiang L, Oner GM et al. miR-34 cooperates with p53 in suppression of prostate cancer by joint regulation of stem cell compartment. Cell Rep 2014; 6: 1000-1007
65. Kojima K, Fujita Y, Nozawa Y, Deguchi T, Ito M. miR34a attenuates paclitaxel-Resistance of hormone-refractory prostate cancer PC3 cells through direct and indirect mechanisms. Prostate 2010; 70: 1501-1512
66. Herr HW, Dotan Z, Donat SM, Bajorin DF. Defining optimal therapy for muscle invasive bladder cancer. J Urol 2007; 177: 437-443
67. Vinall RL, Ripoll AZ, Wang S, Pan CX, deVere White RW. miR34a chemosensitizes bladder cancer cells to cisplatin treatment regardless of p53-Rb pathway status. Int J Cancer 2011; 130: 2526-2538
68. Hoque MO, Lee CC, Cairns P, Schoenberg M, Sidransky D. Genome-Wide genetic characterization of bladder cancer: A comparison of high-Density single-Nucleotide polymorphism arrays and PCR-Based microsatellite analysis. Cancer Res 2003; 63: 2216-2222
69. Yu DS, Hsieh DS, Chang SY. Detection of chromosomal alterations in bladder cancer by comparative genomic hybridization. BJU Int 2001; 87: 889-893
70. Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet 2007; 369: 2106-2120
71. Bown N, Cotterill S, Lastowska M, O'Neill S, Pearson AD, Plantaz D et al. Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N Engl J Med 1999; 340: 1954-1961
72. Attiyeh EF, London WB, Mosse YP, Wang Q, Winter C, Khazi D et al. Chromosome 1p and 11q deletions and outcome in neuroblastoma. N Engl J Med 2005; 353: 2243-2253
73. Kristina AC, Edward FA, Yael PM, Michael JL, Sharon JD, Garrett MB et al. A functional screen identifies miR34a as a candidate neuroblastoma tumor suppressor gene. Mol Cancer Res 2008; 6: 735-742
74. Tivnan A, Tracey L, Buckley PG, Alcock LC, Davidoff AM, Stallings RL. MicroRNA-34a is a potent tumor suppressor molecule in vivo in neuroblastoma. BMC Cancer 2011; 25: 11:33
75. Feinberg-Gorenshtein G, Avigad S, Jeison M, Halevy-Berco G, Mardoukh J, Luria D et al. Reduced levels of miR34a in neuroblastoma are not caused by mutations in the TP53 binding site. Genes Chromosomes Cancer 2009; 48: 539-543
76. Gaur A, Jewell DA, Liang Y, Ridzon D, Moore JH, Chen C et al. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res 2007; 67: 2456-2468
77. Luan S, Sun L, Huang F. MicroRNA-34a: A novel tumor suppressor in p53-Mutant glioma cell line U251. Arch Med Res 2010; 41: 67-74
78. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, Schiff D et al. MicroRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 2010; 15: 1031-1036
79. Massague J. TGFbeta in cancer. Cell 2008; 134: 215-230
80. ten Dijke P, Hill CS. New insights into TGF-b-Smad signalling. Trends Biochem Sci 2004; 29: 265-273.
81. Genovese G, Ergun A, Shukla SA, Campos B, Hanna J, Ghosh P et al. MicroRNA regulatory network inference identifies miR34a as a novel regulator of TGFb signaling in GBM. Cancer Discov 2012; 2: 736-749
82. Wu J, Wu G, Lv L, Ren YF, Zhang XJ, Xue YF et al. MicroRNA-34a inhibits migration and invasion of colon cancer cells via targeting to Fra-1. Carcinogenesis 2012; 33: 519-528
83. Wang X, Dong K, Gao P, Long M, Lin F, Weng Y et al. microRNA-34a sensitizes lung cancer cell lines to DDP treatment independent of p53 status. Cancer Biother Radiopharm 2013; 28: 45-50
84. Gallardo E, Navarro A, Viñolas N, Marrades RM, Diaz T, Gel B et al. miR34a as a prognostic marker of relapse in surgically resected non-Small-Cell lung cancer. Carcinogenesis 2009; 30: 1903-1909
85. Wiggins FJ, Ruffino L, Kelnar K, Omotola M. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 2010; 70: 5923-5930
86. Di Martino MT, Leone E, Amodio N, Foresta U, Lionetti M, Pitari MR et al. Synthetic miR34a mimics as a novel therapeutic agent for multiple myeloma: In vitro and in vivo evidence. Clin Cancer Res 2012; 18: 6260-6270
87. Yan D, Zhou X, Chen X, Hu DN, Dong XD, Wang J et al. MicroRNA-34a inhibits uveal melanoma cell proliferation and migration through downregulation of c-Met. Invest Ophthalmol Vis Sci 2009; 50: 1559-1565
88. Navarro F, Gutman D, Meire E, Caceres M. miR-34a contributes to megakaryocytic differentiation of K562 cells. Blood 2009; 114: 89
89. Ichimura A, Ruike Y, Terasawa K, Shimizu K, Tsujimoto G. miR34a inhibits cell proliferation by repressing MEK1 during megakaryocytic differentiation of K562. Mol Pharmacol 2010; 77: 1016-1024
90. Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S. Targeting epigenetic regulation of miR34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS One 2011; 6: e24099
91. Yan K, Gao J, Yang T, Ma Q, Qiu X, Fan Q et al. MicroRNA-34a inhibits the proliferation and metastasis of osteosarcoma cells both in vitro and in vivo. PLoS One 2012; 7: e33778
92. Nakatani F, Ferracin M, Manara MC, Ventura S, Del Monaco V, Ferrari S et al. miR34a predicts survival of Ewing's sarcoma patients and directly influences cell chemo-Sensitivity and malignancy. J Pathol 2012; 226: 796-805
93. Corney DC, Hwang CI, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK et al. Frequent downregulation of MiR-34 family in human ovarian cancers. Clin Cancer Res 2010; 16: 1119-1128
94. Trang P, Wiggins JF, Daige CL, 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
95. Bandi N, Vassella E. miR34a 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