Hypoxia represses microRNA biogenesis proteins in breast cancer cells

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Bandara, Veronika ^a   Michael, Michael Z ^a   Gleadle, Jonathan M ^a  

^a FLINDERS MEDICAL CENTRE   (Australia)

Author keywords

Breast cancer; Dicer; Drosha; Hypoxia; MicroRNA; Oxygen

Indexed keywords

DICER; EXPORTIN 5; HYPOXIA INDUCIBLE FACTOR; MICRORNA; NUCLEAR PROTEIN; OXYGENASE; PROTEIN DCGR8; PROTEIN DROSHA; PROTEIN PHD2; PROTEIN TARBP2; UNCLASSIFIED DRUG; ALPHA ACTIN; BETA TUBULIN; DCGR8 PROTEIN; DROSHA PROTEIN; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; HYPOXIA INDUCIBLE FACTOR PROLYL HYDROXYLASE INHIBITOR; MESSENGER RNA; MICRORNA BIOGENESIS PROTEIN; OXYGEN; RIBONUCLEOPROTEIN; TARBP2 PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DEAD BOX PROTEIN; DICER1 PROTEIN, HUMAN; RIBONUCLEASE III;

ARTICLE; BIOGENESIS; BREAST CANCER; CONTROLLED STUDY; FEEDBACK SYSTEM; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; HYPOXIA; NUCLEOTIDE SEQUENCE; RNA SYNTHESIS; BREAST CANCER CELL LINE; CANCER GROWTH; CELL HYPOXIA; DICER GENE; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; IMMUNOBLOTTING; MICROARRAY ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; UMBILICAL VEIN ENDOTHELIAL CELL; BREAST TUMOR; FEMALE; GENETICS; HT 29 CELL LINE; MCF 7 CELL LINE; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; TUMOR CELL LINE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BREAST NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; DEAD-BOX RNA HELICASES; FEMALE; HT29 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MCF-7 CELLS; MICRORNAS; MOLECULAR SEQUENCE DATA; RIBONUCLEASE III;

EID: 84904528236     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-533     Document Type: Article

References (58)

1. Reynolds TY, Rockwell S, Glazer PM. Genetic instability induced by the tumor microenvironment. Cancer Res 1996, 56(24):5754-5757.
2. Thomlinson RH, Gray LH. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br J Cancer 1955, 9(4):539-549. 10.1038/bjc.1955.55, 2073776, 13304213.
3. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989, 49(23):6449-6465.
4. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2(1):38-47. 10.1038/nrc704, 11902584.
5. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004, 23(20):4051-4060. 10.1038/sj.emboj.7600385, 524334, 15372072.
6. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006, 13(12):1097-1101. 10.1038/nsmb1167, 17099701.
7. Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004, 18(24):3016-3027. 10.1101/gad.1262504, 535913, 15574589.
8. Kim VN. MicroRNA precursors in motion: exportin-5 mediates their nuclear export. Trends Cell Biol 2004, 14(4):156-159. 10.1016/j.tcb.2004.02.006, 15134074.
9. Grishok A, Pasquinelli AE, Conte D, Li N, Parrish S, Ha I, Baillie DL, Fire A, Ruvkun G, Mello CC. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 2001, 106(1):23-34. 10.1016/S0092-8674(01)00431-7, 11461699.
10. Hutvagner G, McLachlan J, Pasquinelli AE, Balint E, Tuschl T, Zamore PD. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293(5531):834-838. 10.1126/science.1062961, 11452083.
11. Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 2005, 436(7051):740-744. 10.1038/nature03868, 2944926, 15973356.
12. Haase AD, Jaskiewicz L, Zhang H, Laine S, Sack R, Gatignol A, Filipowicz W. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep 2005, 6(10):961-967. 10.1038/sj.embor.7400509, 1369185, 16142218.
13. Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003, 115(2):209-216. 10.1016/S0092-8674(03)00801-8, 14567918.
14. Lim LP, Lau NC, Weinstein EG, Abdelhakim A, Yekta S, Rhoades MW, Burge CB, Bartel DP. The microRNAs of Caenorhabditis elegans. Genes Dev 2003, 17(8):991-1008. 10.1101/gad.1074403, 196042, 12672692.
15. Zhou H, Huang X, Cui H, Luo X, Tang Y, Chen S, Wu L, Shen N. miR-155 and its star-form partner miR-155* cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 2010, 116(26):5885-5894. 10.1182/blood-2010-04-280156, 20852130.
16. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136(2):215-233. 10.1016/j.cell.2009.01.002, 3794896, 19167326.
17. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 2003, 113(1):25-36. 10.1016/S0092-8674(03)00231-9, 12679032.
18. Xu P, Vernooy SY, Guo M, Hay BA. The Drosophila microRNA Mir-14 suppresses cell death and is required for normal fat metabolism. Curr Biol 2003, 13(9):790-795. 10.1016/S0960-9822(03)00250-1, 12725740.
19. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, Croce CM. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 2002, 99(24):15524-15529. 10.1073/pnas.242606799, 137750, 12434020.
20. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, Croce CM. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A 2004, 101(9):2999-3004. 10.1073/pnas.0307323101, 365734, 14973191.
21. Deng S, Calin GA, Croce CM, Coukos G, Zhang L. Mechanisms of microRNA deregulation in human cancer. Cell Cycle 2008, 7(17):2643-2646. 10.4161/cc.7.17.6597, 18719391.
22. Greither T, Grochola LF, Udelnow A, Lautenschlager C, Wurl P, Taubert H. Elevated expression of microRNAs 155, 203, 210 and 222 in pancreatic tumors is associated with poorer survival. Int J Cancer 2010, 126(1):73-80. 10.1002/ijc.24687, 19551852.
23. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Menard S, Palazzo JP, Rosenberg A, Musiani P, Volinia S, Nenci I, Calin GA, Querzoli P, Negrini M, Croce CM. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005, 65(16):7065-7070. 10.1158/0008-5472.CAN-05-1783, 16103053.
24. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR. MicroRNA expression profiles classify human cancers. Nature 2005, 435(7043):834-838. 10.1038/nature03702, 15944708.
25. 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(16):2202-2207. 10.1101/gad.1444406, 1553203, 16882971.
26. Siomi H, Siomi MC. Posttranscriptional regulation of microRNA biogenesis in animals. Mol Cell 2010, 38(3):323-332. 10.1016/j.molcel.2010.03.013, 20471939.
27. Horikawa Y, Wood CG, Yang H, Zhao H, Ye Y, Gu J, Lin J, Habuchi T, Wu X. Single nucleotide polymorphisms of microRNA machinery genes modify the risk of renal cell carcinoma. Clin Cancer Res 2008, 14(23):7956-7962. 10.1158/1078-0432.CCR-08-1199, 2650498, 19047128.
28. Merritt WM, Lin YG, Han LY, Kamat AA, Spannuth WA, Schmandt R, Urbauer D, Pennacchio LA, Cheng JF, Nick AM, Deavers MT, Mourad-Zeidan A, Wang H, Mueller P, Lenburg ME, Gray JW, Mok S, Birrer MJ, Lopez-Berestein G, Coleman RL, Bar-Eli M, Sood AK. Dicer, Drosha, and outcomes in patients with ovarian cancer. N Engl J Med 2008, 359(25):2641-2650. 10.1056/NEJMoa0803785, 2710981, 19092150.
29. Karube Y, Tanaka H, Osada H, Tomida S, Tatematsu Y, Yanagisawa K, Yatabe Y, Takamizawa J, Miyoshi S, Mitsudomi T, Takahashi T. Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci 2005, 96(2):111-115. 10.1111/j.1349-7006.2005.00015.x, 15723655.
30. Kumar MS, Pester RE, Chen CY, Lane K, Chin C, Lu J, Kirsch DG, Golub TR, Jacks T. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 2009, 23(23):2700-2704. 10.1101/gad.1848209, 2788328, 19903759.
31. Kuehbacher A, Urbich C, Dimmeler S. Targeting microRNA expression to regulate angiogenesis. Trends Pharmacol Sci 2008, 29(1):12-15. 10.1016/j.tips.2007.10.014, 18068232.
32. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M. A microRNA signature of hypoxia. Mol Cell Biol 2007, 27(5):1859-1867. 10.1128/MCB.01395-06, 1820461, 17194750.
33. Marsit CJ, Eddy K, Kelsey KT. MicroRNA responses to cellular stress. Cancer Res 2006, 66(22):10843-10848. 10.1158/0008-5472.CAN-06-1894, 17108120.
34. Caruso P, MacLean MR, Khanin R, McClure J, Soon E, Southgate M, MacDonald RA, Greig JA, Robertson KE, Masson R, Denby L, Dempsie Y, Long L, Morrell NW, Baker AH. Dynamic changes in lung microRNA profiles during the development of pulmonary hypertension due to chronic hypoxia and monocrotaline. Arterioscler Thromb Vasc Biol 2010, 30(4):716-723. 10.1161/ATVBAHA.109.202028, 20110569.
35. Camps C, Buffa FM, Colella S, Moore J, Sotiriou C, Sheldon H, Harris AL, Gleadle JM, Ragoussis J. hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 2008, 14(5):1340-1348. 10.1158/1078-0432.CCR-07-1755, 18316553.
36. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, Gleadle JM. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 2006, 281(22):15215-15226. 10.1074/jbc.M511408200, 16565084.
37. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008, 10(5):593-601. 10.1038/ncb1722, 18376396.
38. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30(1):207-210. 10.1093/nar/30.1.207, 99122, 11752295.
39. Woo KJ, Lee TJ, Park JW, Kwon TK. Desferrioxamine, an iron chelator, enhances HIF-1alpha accumulation via cyclooxygenase-2 signaling pathway. Biochem Biophys Res Commun 2006, 343(1):8-14. 10.1016/j.bbrc.2006.02.116, 16527254.
40. Appelhoff RJ, Tian YM, Raval RR, Turley H, Harris AL, Pugh CW, Ratcliffe PJ, Gleadle JM. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 2004, 279(37):38458-38465. 10.1074/jbc.M406026200, 15247232.
41. Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S, Enzo E, Guzzardo V, Rondina M, Spruce T, Parenti AR, Daidone MG, Bicciato S, Piccolo S. A MicroRNA targeting dicer for metastasis control. Cell 2010, 141(7):1195-1207. 10.1016/j.cell.2010.05.017, 20603000.
42. Forman JJ, Legesse-Miller A, Coller HA. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc Natl Acad Sci U S A 2008, 105(39):14879-14884. 10.1073/pnas.0803230105, 2567461, 18812516.
43. Melo SA, Ropero S, Moutinho C, Aaltonen LA, Yamamoto H, Calin GA, Rossi S, Fernandez AF, Carneiro F, Oliveira C, Ferreira B, Liu CG, Villanueva A, Capella G, Schwartz S, Shiekhattar R, Esteller M. A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nat Genet 2009, 41(3):365-370. 10.1038/ng.317, 19219043.
44. Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 2007, 100(8):1164-1173. 10.1161/01.RES.0000265065.26744.17, 17379831.
45. Ho JJ, Metcalf JL, Yan MS, Turgeon PJ, Wang JJ, Chalsev M, Petruzziello-Pellegrini TN, Tsui AK, He JZ, Dhamko H, Man HS, Robb GB, Teh BT, Ohh M, Marsden PA. Functional importance of Dicer protein in the adaptive cellular response to hypoxia. J Biol Chem 2012, 287(34):29003-29020. 10.1074/jbc.M112.373365, 3436557, 22745131.
46. Bu Y, Lu C, Bian C, Wang J, Li J, Zhang B, Li Z, Brewer G, Zhao RC. Knockdown of Dicer in MCF-7 human breast carcinoma cells results in G1 arrest and increased sensitivity to cisplatin. Oncol Rep 2009, 21(1):13-17.
47. Wu C, So J, Davis-Dusenbery BN, Qi HH, Bloch DB, Shi Y, Lagna G, Hata A. Hypoxia potentiates microRNA-mediated gene silencing through posttranslational modification of Argonaute2. Mol Cell Biol 2011, 31(23):4760-4774. 10.1128/MCB.05776-11, 3232924, 21969601.
48. Camps C, Saini HK, Mole DR, Choudhry H, Reczko M, Guerra-Assuncao JA, Tian YM, Buffa FM, Harris AL, Hatzigeorgiou AG, Enright AJ, Ragoussis J. Integrated analysis of microRNA and mRNA expression and association with HIF binding reveals the complexity of microRNA expression regulation under hypoxia. Mol Cancer 2014, 13:28. 10.1186/1476-4598-13-28, 3928101, 24517586.
49. Romero-Ruiz A, Bautista L, Navarro V, Heras-Garvin A, March-Diaz R, Castellano A, Gomez-Diaz R, Castro MJ, Berra E, Lopez-Barneo J, Pascual A. Prolyl hydroxylase-dependent modulation of eukaryotic elongation factor 2 activity and protein translation under acute hypoxia. J Biol Chem 2012, 287(12):9651-9658. 10.1074/jbc.M111.299180, 3308822, 22308030.
50. Kulshreshtha R, Ferracin M, Negrini M, Calin GA, Davuluri RV, Ivan M. Regulation of microRNA expression: the hypoxic component. Cell Cycle 2007, 6(12):1426-1431.
51. Han J, Pedersen JS, Kwon SC, Belair CD, Kim YK, Yeom KH, Yang WY, Haussler D, Blelloch R, Kim VN. Posttranscriptional crossregulation between Drosha and DGCR8. Cell 2009, 136(1):75-84. 10.1016/j.cell.2008.10.053, 2680683, 19135890.
52. Smibert P, Yang JS, Azzam G, Liu JL, Lai EC. Homeostatic control of Argonaute stability by microRNA availability. Nat Struct Mol Biol 2013, 20:789-795. 10.1038/nsmb.2606, 3702675, 23708604.
53. Voellenkle C, Rooij J, Guffanti A, Brini E, Fasanaro P, Isaia E, Croft L, David M, Capogrossi MC, Moles A, Felsani A, Martelli F. Deep-sequencing of endothelial cells exposed to hypoxia reveals the complexity of known and novel microRNAs. RNA 2012, 18(3):472-484. 10.1261/rna.027615.111, 3285935, 22282338.
54. Yang JS, Lai EC. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 2011, 43(6):892-903. 10.1016/j.molcel.2011.07.024, 3176435, 21925378.
55. Gantier MP, McCoy CE, Rusinova I, Saulep D, Wang D, Xu D, Irving AT, Behlke MA, Hertzog PJ, Mackay F, Williams BR. Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res 2011, 39(13):5692-5703. 10.1093/nar/gkr148, 3141258, 21447562.
56. Langenberger D, Cakir MV, Hoffmann S, Stadler PF. Dicer-processed small RNAs: rules and exceptions. J Exp Zool B Mol Dev Evol 2012, 320(1):35-46.
57. Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, Wolfe SA, Giraldez AJ. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 2010, 328(5986):1694-1698. 10.1126/science.1190809, 3093307, 20448148.
58. Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465(7298):584-589. 10.1038/nature09092, 2995450, 20424607.