Dysregulation of microRNA biogenesis in cancer: The impact of mutant p53 on Drosha complex activity

Journal of Experimental and Clinical Cancer Research

Volumn 35, Issue 1, 2016, Pages

  Gurtner, Aymone ^a   Falcone, Emmanuela ^a   Garibaldi, Francesca ^a   Piaggio, Giulia ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Biogenesis; Drosha; Microprocessor complex; miRNA; mutp53; p68; p72

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 105; MICRORNA 107; MICRORNA 128 2; MICRORNA 130B; MICRORNA 141; MICRORNA 142; MICRORNA 143; MICRORNA 145; MICRORNA 155; MICRORNA 16; MICRORNA 18A; MICRORNA 206; MICRORNA 218; MICRORNA 223; MICRORNA 26A; MICRORNA 27A; MICRORNA 515; MICRORNA 517A; MICRORNA 518B; MICRORNA 519A; MICRORNA 519C; MICRORNA 520G; MICRORNA 582; MICRORNA 628; PROTEIN P53; RIBONUCLEASE; RIBONUCLEASE DROSHA; UNCLASSIFIED DRUG; DROSHA PROTEIN, HUMAN; RIBONUCLEASE III; TP53 PROTEIN, HUMAN;

APOPTOSIS; BIOGENESIS; CANCER CELL; CANCER INHIBITION; CARCINOGENESIS; CELL CYCLE ARREST; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; METASTASIS; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA PROCESSING; RNA TRANSCRIPTION; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; UPREGULATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MUTATION; SIGNAL TRANSDUCTION;

GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HUMANS; MICRORNAS; MUTATION; NEOPLASMS; RIBONUCLEASE III; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84960532706     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/s13046-016-0319-x     Document Type: Review

References (93)

1. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014;15:509-24.
2. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. 2010;11:597-610.
3. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: MicroRNA biogenesis pathways and their regulation. Nat Cell Biol. 2009;11:228-34.
4. Bushati N, Cohen SM. microRNA functions. Annu Rev Cell Dev Biol. 2007;23:175-205.
5. Lujambio A, Lowe SW. The microcosmos of cancer. Nature. 2012;482:347-55.
6. Lynam-Lennon N, Maher SG, Reynolds JV. The roles of microRNA in cancer and apoptosis. Biol Rev Camb Philos Soc. 2009;84:55-71.
7. Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A, et al. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res. 2005;33:2697-706.
8. 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.
9. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol. 2006;13:1097-101.
10. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature. 2003;425:415-9.
11. Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, et al. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell. 2006;125:887-901.
12. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, et al. The Microprocessor complex mediates the genesis of microRNAs. Nature. 2004;432:235-40.
13. Zeng Y, Cullen BR. Structural requirements for premicroRNA binding and nuclear export by Exportin 5. Nucleic Acids Res. 2004;32:4776-85.
14. Lee Y, Hur I, Park SY, Kim YK, Suh MR, Kim VN, et al. The role of PACT in the RNA silencing pathway. EMBO J. 2006;25:522-32.
15. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, et al. Mammalian microRNAs: Experimental evaluation of novel and previously annotated genes. Genes Dev. 2010;24:992-1009.
16. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell. 2009;136:215-33.
17. Jansson MD, Lund AH. MicroRNA and cancer. Mol Oncol. 2012;6:590-610.
18. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet. 2009;10:704-14.
19. Lu J, Getz G. MicroRNA expression profiles classify human cancers. Nature. 2005;435:834-8.
20. Munker R, Calin GA. MicroRNA profiling in cancer. Clin Sci (Lond). 2011;121:141-58.
21. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 2006;9:189-98.
22. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353:1793-801.
23. Iorio MV, Croce CM. MicroRNA dysregulation in cancer: Diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med. 2012;4:143-59.
24. Van Kouwenhove M, Kedde M, Agami R. MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer. 2011;11:644-56.
25. Fabbri M, Ivan M, Cimmino A, Negrini M, Calin GA. Regulatory mechanisms of microRNAs involvement in cancer. Expert Opin Biol Ther. 2007;7:1009-19.
26. 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 USA. 2004;101:2999-3004.
27. Lagana A, Russo F, Sismeiro C, Giugno R, Pulvirenti A, Ferro A. Variability in the incidence of miRNAs and genes in fragile sites and the role of repeats and CpG islands in the distribution of genetic material. PLoS One. 2010;5:e11166.
28. Mayr C, Hemann MT, Bartel DP. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science. 2007;315:1576-9.
29. Romero-Cordoba SL, Salido-Guadarrama I, Rodriguez-Dorantes M, Hidalgo-Miranda A. miRNA biogenesis: Biological impact in the development of cancer. Cancer Biol Ther. 2014;15(11):1444-55.
30. Liu X, Chen X, Yu X, Tao Y, Bode AM, Dong Z, et al. Regulation of microRNAs by epigenetics and their interplay involved in cancer. J Exp Clin Cancer Res. 2013;32:96. doi: 10.1186/1756-9966-32-96.
31. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 2006;20:2202-7.
32. Hill DA, Ivanovich J, Priest JR, Gurnett CA, Dehner LP, Desruisseau D, et al. DICER1 mutations in familial pleuropulmonary blastoma. Science. 2009;325(5943):965.
33. Melo SA, Moutinho C, Ropero S, Calin GA, Rossi S, Spizzo R, et al. A genetic defect in exportin-5 traps precursor microRNAs in the nucleus of cancer cells. Cancer Cell. 2010;18:303-15.
34. Melo SA, Ropero S, Moutinho C, Aaltonen LA, Yamamoto H, Calin GA, et al. A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nat Genet. 2009;41:365-70.
35. Wegert J, Ishaque N, Vardapour R, Geörg C, Gu Z, Bieg M, et al. Mutations in the SIX1/2 pathway and the DROSHA/DGCR8 miRNA microprocessor complex underlie high-risk blastemal type Wilms tumors. Cancer Cell. 2015;27(2):298-311.
36. Walz AL, Ooms A, Gadd S, Gerhard DS, Smith MA, Guidry Auvil JM, et al. Recurrent DGCR8, DROSHA, and SIX homeodomain mutations in favorable histology Wilms tumors. Cancer Cell. 2015;27(2):286-97.
37. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet. 2007;39:673-7.
38. Fuller-Pace FV, Moore HC. RNA helicases p68 and p72: Multifunctional proteins with important implications for cancer development. Future Oncol. 2011;7:239-51.
39. Hong S, Noh H, Chen H, Padia R, Pan ZK, Su SB, et al. Signaling by p38 MAPK stimulates nuclear localization of the microprocessor component p68 for processing of selected primary microRNAs. Sci Signaling. 2013;6:ra16.
40. Han C, Liu Y, Wan G, Choi HJ, Zhao L, Ivan C, et al. The RNA-binding protein DDX1 promotes primary microRNA maturation and inhibits ovarian tumor progression. Cell Rep. 2014;8(5):1447-60.
41. Kawai S, Amano A. BRCA1 regulates microRNA biogenesis via the DROSHA microprocessor complex. J Cell Biol. 2012;197:201-8.
42. Gruber JJ, Zatechka DS, Sabin LR, Yong J, Lum JJ, Kong M, et al. Ars2 links the nuclear cap-binding complex to RNA interference and cell proliferation. Cell. 2009;138:328-39.
43. Sabin LR, Zhou R, Gruber JJ, Lukinova N, Bambina S, Berman A, et al. Ars2 regulates both miRNA- A nd siRNA-dependent silencing and suppresses RNA virus infection in Drosophila. Cell. 2009;138:340-51.
44. Nemlich Y, Greenberg E, Ortenberg R, Besser MJ, Barshack I, Jacob-Hirsch J, et al. MicroRNA-mediated loss of ADAR1 in metastatic melanoma promotes tumor growth. J Clin Invest. 2013;123:2703-18.
45. Haselmann V, Kurz A, Bertsch U, Hubner S, Olempska-Muller M, Fritsch J, et al. Nuclear death receptor TRAIL-R2 inhibits maturation of let-7 and promotes proliferation of pancreatic and other tumor cells. Gastroenterology. 2014;146:278-90.
46. Michlewski G, Guil S, Semple CA, Caceres JF. Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell. 2008;32:383-93.
47. Heo I, Joo C, Kim YK, Ha M, Yoon MJ, Cho J, et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through premicroRNA uridylation. Cell. 2009;138:696-708.
48. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature. 2008;454:56-61.
49. Mori M, Triboulet R, Mohseni M, Schlegelmilch K, Shrestha K, Camargo FD, et al. Hippo signaling regulates microprocessor and links cell-density-dependent miRNA biogenesis to cancer. Cell. 2014;156:893-906.
50. Paris O, Ferraro L, Grober OM, Ravo M, De Filippo MR, Giurato G, et al. Direct regulation of microRNA biogenesis and expression by estrogen receptor beta in hormone-responsive breast cancer. Oncogene. 2012;31(38):4196-206.
51. Dai TY, Cao L, Yang ZC, Li YS, Tan L, Ran XZ, et al. P68 RNA helicase as a molecular target for cancer therapy. J Exp Clin Cancer Res. 2014;33:64. doi: 10.1186/s13046-014-0064-y.
52. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K. Modulation of microRNA processing by p53. Nature. 2009;460:529-33.
53. Nakazawa K, Dashzeveg N, Yoshida K. Tumor suppressor p53 induces miR-1915 processing to inhibit Bcl-2 in the apoptotic response to DNA damage. FEBS J. 2014;281(13):2937-44.
54. Chang J, Davis-Dusenbery BN, Kashima R, Jiang X, Marathe N, Sessa R, et al. Acetylation of p53 stimulates miRNA processing and determines cell survival following genotoxic stress. EMBO J. 2013;32(24):3192-205.
55. Herbert KJ, Cook AL, Snow ET. SIRT1 modulates miRNA processing defects in p53-mutated human keratinocytes. J Dermatol Sci. 2014;74(2):142-9.
56. Jiang FZ, He YY, Wang HH, Zhang HL, Zhang J, Yan XF, et al. Mutant p53 induces EZH2 expression and promotes epithelial-mesenchymal transition by disrupting p68-Drosha complex assembly and attenuating miR-26a processing. Oncotarget. 2015. doi: 10.18632/oncotarget.6350.
57. Garibaldi F, Falcone E, Trisciuoglio D, Colombo T, Lisek K, Walerych D, Del Sal G, Paci P, Bossi G, Piaggio G, Gurtner A. Mutant p53 inhibits miRNA biogenesis by interfering with the Microprocessor complex. Oncogene. In press.
58. Li CL, Yeh KH, Liu WH, Chen CL, Chen DS, Chen PJ, et al. Elevated p53 promotes the processing of miR-18a to decrease estrogen receptor-α in female hepatocellular carcinoma. Int J Cancer. 2015;136(4):761-70.
59. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, et al. The microprocessor complex mediates the genesis of MicroRNAs. Nature. 2004;432:235-40.
60. Muller PA, Vousden KH. Mutant p53 in cancer: New functions and therapeutic opportunities. Cancer Cell. 2014;25:304-17.
61. Oren M. Decision making by p53: Life, death and cancer. Cell Death Differ. 2003;10:431-42.
62. Gurtner A, Starace G, Norelli G, Piaggio G, Sacchi A, Bossi G. Mutant p53-induced up-regulation of mitogen-activated protein kinase kinase 3 contributes to gain of function. J Biol Chem. 2010;285(19):14160-9.
63. Ubertini V, Norelli G, D'Arcangelo D, Gurtner A, Cesareo E, Baldari S, et al. Mutant p53 gains new function in promoting inflammatory signals by repression of the secreted interleukin-1 receptor antagonist. Oncogene. 2015;34(19):2493-504.
64. Donehower LA, Lozano G. 20 years studying p53 functions in genetically engineered mice. Nat Rev Cancer. 2009;9:831-41.
65. Donehower LA. Insights into wild-type and mutant p53 functions provided by genetically engineered mice. Hum Mutat. 2014;35:715-27.
66. Gurtner A, Starace G, Norelli G, Piaggio G, Sacchi A, Bossi G. Mutant p53-induced up-regulation of mitogen-activated protein kinase kinase 3 contributes to gain of function. J Biol Chem. 2010;285:14160-9.
67. Zhang X, Wan G, Berger FG, He X, Lu X. The ATM kinase induces microRNA biogenesis in the DNA damage response. Mol Cell. 2011;41(4):371-83.
68. Yamakuchi M, Lowenstein CJ. MiR-34, SIRT1 and p53: The feedback loop. Cell Cycle. 2009;8:712-5.
69. Léveillé N, Elkon R, Davalos V, Manoharan V, Hollingworth D, Oude Vrielink J, et al. Selective inhibition of microRNA accessibility by RBM38 is required for p53 activity. Nat Commun. 2011;2:513. doi: 10.1038/ncomms1519.
70. Deb G, Singh AK, Gupta S. EZH2: Not EZHY (easy) to deal. Mol Cancer Res. 2014;12:639-53. doi: 10.1158/1541-7786.
71. Deng L, Yang H, Tang J, Lin Z, Yin A, Gao Y, et al. Inhibition of MTA1 by ERα contributes to protection hepatocellular carcinoma from tumor proliferation and metastasis. J Exp Clin Cancer Res. 2015;34:128. doi: 10.1186/s13046-015-0248-0.
72. 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.
73. Mu P, Han YC, Betel D, Yao E, Squatrito M, Ogrodowski P, et al. Genetic dissection of the miR-17 ∼92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev. 2009;23:2806-11.
74. Feng Y, Liu J, Kang Y, He Y, Liang B, Yang P, et al. miR-19a acts as an oncogenic microRNA and is up-regulated in bladder cancer. J Exp Clin Cancer Res. 2014;33:67. doi: 10.1186/PREACCEPT-9242556491295527.
75. Wang W, Cheng B, Miao L, Mei Y, Wu M. Mutant p53-R273H gains new function in sustained activation of EGFR signaling via suppressing miR-27a expression. Cell Death Dis. 2013;4:e574.
76. Subramanian M, Francis P, Bilke S, Li XL, Hara T, Lu X, et al. A mutant p53/let-7i-axis-regulated gene network drives cell migration, invasion and metastasis. Oncogene. 2015;34(9):1094-104.
77. Dong P, Karaayvaz M, Jia N, Kaneuchi M, Hamada J, Watari H, et al. Mutant p53 gain-of-function induces epithelial-mesenchymal transition through modulation of the miR-130b-ZEB1 axis. Oncogene. 2013;32(27):3286-95.
78. Neilsen PM, Noll JE, Mattiske S, Bracken CP, Gregory PA, Schulz RB, et al. Mutant p53 drives invasion in breast tumors through up-regulation ofmiR-155. Oncogene. 2013;32(24):2992-3000.
79. Donzelli S, Fontemaggi G, Fazi F, Di Agostino S, Padula F, Biagioni F, et al. MicroRNA-128-2 targets the transcriptional repressor E2F5 enhancing mutant p53 gain of function. Cell Death Differ. 2012;19(6):1038-48.
80. Masciarelli S, Fontemaggi G, Di Agostino S, Donzelli S, Carcarino E, Strano S, et al. Gain-of-function mutant p53 downregulates miR-223 contributing to chemoresistance of cultured tumor cells. Oncogene. 2014;33(12):1601-8.
81. Zhang Y, Geng L, Talmon G, Wang J. MicroRNA-520 g confers drug resistance by regulating p21 expression in colorectal cancer. J Biol Chem. 2015;290(10):6215-25.
82. Zhang M, Zhou S, Zhang L, Zhang J, Cai H, Zhu J, et al. miR-518b is down-regulated, and involved in cell proliferation and invasion by targeting Rap1b in esophageal squamous cell carcinoma. FEBS Lett. 2012;586:3508-21.
83. Zhang X, Zhang Y, Yang J, Li S, Chen J. Upregulation of miR-582-5p inhibits cell proliferation, cell cycle progression and invasion by targeting Rab27a in human colorectal carcinoma. Cancer Gene Ther. 2015;22(10):475-80.
84. Feng X, Wang Z, Fillmore R, Xi Y. MiR-200, a new star miRNA in human cancer. Cancer Lett. 2014;344:166-73.
85. Cha ST, Chen PS, Johansson G, Chu CY, Wang MY, Jeng YM, et al. MicroRNA-519c suppresses hypoxia-inducible factor-1alpha expression and tumor angiogenesis. Cancer Res. 2010;70:2675-85.
86. Borralho PM, Simões AE, Gomes SE, Lima RT, Carvalho T, et al. miR-143 overexpression impairs growth of human colon carcinoma xenografts in mice with induction of apoptosis and inhibition of proliferation. PLoS One. 2011;6:e23787. doi: 10.1371/journal.pone.0023787.
87. Zhang J, Sun Q, Zhang Z, Ge S, Han ZG, Chen WT, et al. Loss of microRNA-143/145 disturbs cellular growth and apoptosis of human epithelial cancers by impairing the MDM2-p53 feedback loop. Oncogene. 2013;32:61-9. doi: 10.1038/onc.2012.28.
88. Wu L, Cai C, Wang X, Liu M, Li X, Tang H. MicroRNA-142-3p, a new regulator of RAC1, suppresses the migration and invasion of hepatocellular carcinoma cells. FEBS Lett. 2011;585:1322-30.
89. Liu RF, Xu X, Huang J, Fei QL, Chen F, Li YD, et al. Down-regulation of miR-517a and miR-517c promotes proliferation of hepatocellular carcinoma cells via targeting Pyk2. Cancer Lett. 2013;329:164-73.
90. Tu Y, Gao X, Li G, Fu H, Cui D, Liu H, et al. MicroRNA-218 inhibits glioma invasion, migration, proliferation, and cancer stem-like cell self-renewal by targeting the polycomb group gene Bmi1. Cancer Res. 2013;73:6046-55.
91. Abdelmohsen K, Kim MM, Srikantan S, Mercken EM, Brennan SE, Wilson GM, et al. miR-519 suppresses tumor growth by reducing HuR levels. Cell Cycle. 2010;9(7):1354-9.
92. Pinho FG, Frampton AE, Nunes J, Krell J, Alshaker H, et al. Downregulation of microRNA-515-5p by the estrogen receptor modulates sphingosine kinase 1 and breast cancer cell proliferation. Cancer Res. 2013;73:5936-48.
93. Nohata N, Hanazawa T, Enokida H, Seki N. microRNA-1/133a and microRNA-206/133b clusters: Dysregulation and functional roles in human cancers. Oncotarget. 2012;3:9-21.