MRNA expression profiles show differential regulatory effects of microRNAs between estrogen receptor-positive and estrogen receptor-negative breast cancer

Genome Biology

Volumn 10, Issue 9, 2009, Pages

  Cheng, Chao ^a   Fu, Xuping ^b   Alves, Pedro ^a   Gerstein, Mark ^a,c  

^a YALE UNIVERSITY   (United States)

^b FUDAN UNIVERSITY   (China)

^c Yale University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; DICER; ESTROGEN RECEPTOR; MESSENGER RNA; MICRORNA; EIF2C1 PROTEIN, HUMAN; EIF2C2 PROTEIN, HUMAN; INITIATION FACTOR; INITIATION FACTOR 2; RIBONUCLEASE III;

ARTICLE; BIOINFORMATICS; BREAST CANCER; CANCER CLASSIFICATION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; PREDICTION; RNA PROCESSING; ALGORITHM; BREAST TUMOR; DNA MICROARRAY; FEMALE; GENETICS; HUMAN; METABOLISM; METHODOLOGY;

ALGORITHMS; BREAST NEOPLASMS; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTORS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, ESTROGEN; RIBONUCLEASE III; RNA, MESSENGER;

EID: 76249103552     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-9-r90     Document Type: Article

References (73)

1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
2. Ambros V. microRNAs: tiny regulators with great potential. Cell 2001, 107:823-826. 10.1016/S0092-8674(01)00616-X, 11779458.
3. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20. 10.1016/j.cell.2004.12.035, 15652477.
4. Cheng AM, Byrom MW, Shelton J, Ford LP. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 2005, 33:1290-1297. 10.1093/nar/gki200, 552951, 15741182.
5. Xu P, Guo M, Hay BA. MicroRNAs and the regulation of cell death. Trends Genet 2004, 20:617-624. 10.1016/j.tig.2004.09.010, 15522457.
6. Karp X, Ambros V. Developmental biology. Encountering microRNAs in cell fate signaling. Science 2005, 310:1288-1289. 10.1126/science.1121566, 16311325.
7. Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004, 303:83-86. 10.1126/science.1091903, 14657504.
8. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006, 6:857-866. 10.1038/nrc1997, 17060945.
9. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006, 6:259-269. 10.1038/nrc1840, 16557279.
10. 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 USA 2004, 101:2999-3004. 10.1073/pnas.0307323101, 365734, 14973191.
11. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647. 10.1016/j.cell.2005.01.014, 15766527.
12. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu CG, Kipps TJ, Negrini M, Croce CM. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005, 102:13944-13949. 10.1073/pnas.0506654102, 1236577, 16166262.
13. 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, 435:834-838. 10.1038/nature03702, 15944708.
14. Rosenfeld N, Aharonov R, Meiri E, Rosenwald S, Spector Y, Zepeniuk M, Benjamin H, Shabes N, Tabak S, Levy A, Lebanony D, Goren Y, Silberschein E, Targan N, Ben-Ari A, Gilad S, Sion-Vardy N, Tobar A, Feinmesser M, Kharenko O, Nativ O, Nass D, Perelman M, Yosepovich A, Shalmon B, Polak-Charcon S, Fridman E, Avniel A, Bentwich I, Bentwich Z, et al. MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 2008, 26:462-469. 10.1038/nbt1392, 18362881.
15. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906. 10.1038/35002607, 10706289.
16. Pillai RS, Bhattacharyya SN, Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms?. Trends Cell Biol 2007, 17:118-126. 10.1016/j.tcb.2006.12.007, 17197185.
17. Farh KK, Grimson A, Jan C, Lewis BP, Johnston WK, Lim LP, Burge CB, Bartel DP. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 2005, 310:1817-1821. 10.1126/science.1121158, 16308420.
18. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 2005, 123:1133-1146. 10.1016/j.cell.2005.11.023, 16337999.
19. Xie X, Lu J, Kulbokas EJ, Golub TR, Mootha V, Lindblad-Toh K, Lander ES, Kellis M. Systematic discovery of regulatory motifs in human promoters and 3' UTRs by comparison of several mammals. Nature 2005, 434:338-345. 10.1038/nature03441, 15735639.
20. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005, 438:685-689. 10.1038/nature04303, 16258535.
21. Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, Pasquinelli AE. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 2005, 122:553-563. 10.1016/j.cell.2005.07.031, 16122423.
22. Wu L, Fan J, Belasco JG. MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci USA 2006, 103:4034-4039. 10.1073/pnas.0510928103, 1449641, 16495412.
23. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773. 10.1038/nature03315, 15685193.
24. Wang X. Systematic identification of microRNA functions by combining target prediction and expression profiling. Nucleic Acids Res 2006, 34:1646-1652. 10.1093/nar/gkl068, 1405822, 16549876.
25. Arora A, Simpson DA. Individual mRNA expression profiles reveal the effects of specific microRNAs. Genome Biol 2008, 9:R82. 10.1186/gb-2008-9-5-r82, 2441468, 18485210.
26. Cheng C, Li LM. Inferring microRNA activities by combining gene expression with microRNA target prediction. PLoS ONE 2008, 3:e1989. 10.1371/journal.pone.0001989, 2291556, 18431476.
27. Yu Z, Jian Z, Shen SH, Purisima E, Wang E. Global analysis of microRNA target gene expression reveals that miRNA targets are lower expressed in mature mouse and Drosophila tissues than in the embryos. Nucleic Acids Res 2007, 35:152-164. 10.1093/nar/gkl1032, 1802562, 17158157.
28. Hartmann LC, Sellers TA, Schaid DJ, Nayfield S, Grant CS, Bjoraker JA, Woods J, Couch F. Clinical options for women at high risk for breast cancer. Surg Clin North Am 1999, 79:1189-1206. 10.1016/S0039-6109(05)70068-2, 10572558.
29. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006, 103:2257-2261. 10.1073/pnas.0510565103, 1413718, 16461460.
30. Blenkiron C, Goldstein LD, Thorne NP, Spiteri I, Chin SF, Dunning MJ, Barbosa-Morais NL, Teschendorff AE, Green AR, Ellis IO, Tavare S, Caldas C, Miska EA. MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol 2007, 8:R214. 10.1186/gb-2007-8-10-r214, 2246288, 17922911.
31. 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, 65:7065-7070. 10.1158/0008-5472.CAN-05-1783, 16103053.
32. Mattie MD, Benz CC, Bowers J, Sensinger K, Wong L, Scott GK, Fedele V, Ginzinger D, Getts R, Haqq C. Optimized high-throughput microRNA expression profiling provides novel biomarker assessment of clinical prostate and breast cancer biopsies. Mol Cancer 2006, 5:24. 10.1186/1476-4598-5-24, 1563474, 16784538.
33. Perou CM, Sorlie T, Eisen MB, Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D. Molecular portraits of human breast tumours. Nature 2000, 406:747-752. 10.1038/35021093, 10963602.
34. van't Veer LJ, Dai H, Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536. 10.1038/415530a, 11823860.
35. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J, Lindahl T, Pawitan Y, Hall P, Nordgren H, Wong JE, Liu ET, Bergh J, Kuznetsov VA, Miller LD. Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 2006, 66:10292-10301. 10.1158/0008-5472.CAN-05-4414, 17079448.
36. Pawitan Y, Bjohle J, Amler L, Borg AL, Egyhazi S, Hall P, Han X, Holmberg L, Huang F, Klaar S, Liu ET, Miller L, Nordgren H, Ploner A, Sandelin K, Shaw PM, Smeds J, Skoog L, Wedren S, Bergh J. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res 2005, 7:R953-964. 10.1186/bcr1325, 1410752, 16280042.
37. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein Lonning P, Borresen-Dale AL. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874. 10.1073/pnas.191367098, 58566, 11553815.
38. Miller LD, Smeds J, George J, Vega VB, Vergara L, Ploner A, Pawitan Y, Hall P, Klaar S, Liu ET, Bergh J. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci USA 2005, 102:13550-13555. 10.1073/pnas.0506230102, 1197273,1197273, 16141321.
39. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524. 10.1038/nature03799, 1283098, 16049480.
40. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, Jatkoe T, Berns EM, Atkins D, Foekens JA. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005, 365:671-679.
41. Richardson AL, Wang ZC, De Nicolo A, Lu X, Brown M, Miron A, Liao X, Iglehart JD, Livingston DM, Ganesan S. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 2006, 9:121-132. 10.1016/j.ccr.2006.01.013, 16473279.
42. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98:5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
43. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. The role of site accessibility in microRNA target recognition. Nat Genet 2007, 39:1278-1284. 10.1038/ng2135, 17893677.
44. Hess KR, Anderson K, Symmans WF, Valero V, Ibrahim N, Mejia JA, Booser D, Theriault RL, Buzdar AU, Dempsey PJ, Rouzier R, Sneige N, Ross JS, Vidaurre T, Gomez HL, Hortobagyi GN, Pusztai L. Pharmacogenomic predictor of sensitivity to preoperative chemotherapy with paclitaxel and fluorouracil, doxorubicin, and cyclophosphamide in breast cancer. J Clin Oncol 2006, 24:4236-4244. 10.1200/JCO.2006.05.6861, 16896004.
45. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500. 10.1038/ng1536, 15806104.
46. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS Biol 2004, 2:e363. 10.1371/journal.pbio.0020363, 521178, 15502875.
47. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003, 115:787-798. 10.1016/S0092-8674(03)01018-3, 14697198.
48. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007, 27:91-105. 10.1016/j.molcel.2007.06.017, 17612493.
49. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008, 455:64-71. 10.1038/nature07242, 18668037.
50. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 10.1016/j.cell.2009.01.002, 19167326.
51. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009, 19:92-105. 10.1101/gr.082701.108, 2612969, 18955434.
52. Adams BD, Furneaux H, White BA. The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-alpha (ERalpha) and represses ERalpha messenger RNA and protein expression in breast cancer cell lines. Mol Endocrinol 2007, 21:1132-1147. 10.1210/me.2007-0022, 17312270.
53. 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, 359:2641-2650. 10.1056/NEJMoa0803785, 2710981, 19092150.
54. Chiosea S, Jelezcova E, Chandran U, Luo J, Mantha G, Sobol RW, Dacic S. Overexpression of Dicer in precursor lesions of lung adenocarcinoma. Cancer Res 2007, 67:2345-2350. 10.1158/0008-5472.CAN-06-3533, 17332367.
55. 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, 96:111-115. 10.1111/j.1349-7006.2005.00015.x, 15723655.
56. Wiesen JL, Tomasi TB. Dicer is regulated by cellular stresses and interferons. Mol Immunol 2009, 46:1222-1228. 10.1016/j.molimm.2008.11.012, 19118902.
57. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006, 125:1111-1124. 10.1016/j.cell.2006.04.031, 16777601.
58. Marsit CJ, Eddy K, Kelsey KT. MicroRNA responses to cellular stress. Cancer Res 2006, 66:10843-10848. 10.1158/0008-5472.CAN-06-1894, 17108120.
59. Ketting RF, Fischer SE, Bernstein E, Sijen T, Hannon GJ, Plasterk RH. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 2001, 15:2654-2659. 10.1101/gad.927801, 312808, 11641272.
60. 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, 436:740-744. 10.1038/nature03868, 15973356.
61. Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007, 131:1097-1108. 10.1016/j.cell.2007.10.032, 18083100.
62. 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, 6:961-967. 10.1038/sj.embor.7400509, 1369185, 16142218.
63. MacRae IJ, Ma E, Zhou M, Robinson CV, Doudna JA. In vitro reconstitution of the human RISC-loading complex. Proc Natl Acad Sci USA 2008, 105:512-517. 10.1073/pnas.0710869105, 2206567, 18178619.
64. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004, 15:185-197. 10.1016/j.molcel.2004.07.007, 15260970.
65. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 2007, 39:673-677. 10.1038/ng2003, 17401365.
66. Adams BD, Claffey KP, White BA. Argonaute-2 expression is regulated by epidermal growth factor receptor and mitogen-activated protein kinase signaling and correlates with a transformed phenotype in breast cancer cells. Endocrinology 2009, 150:14-23. 10.1210/en.2008-0984, 18787018.
67. Salomon DS, Bianco C, De Santis M. Cripto: a novel epidermal growth factor (EGF)-related peptide in mammary gland development and neoplasia. Bioessays 1999, 21:61-70. 10.1002/(SICI)1521-1878(199901)21:1<61::AID-BIES8>3.0.CO;2-H, 10070255.
68. McKay MM, Morrison DK. Integrating signals from RTKs to ERK/MAPK. Oncogene 2007, 26:3113-3121. 10.1038/sj.onc.1210394, 17496910.
69. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001, 2:127-137. 10.1038/35052073, 11252954.
70. Adams BD, Cowee DM, White BA. The role of miR-206 in the epidermal growth factor (EGF) induced repression of estrogen receptor-alpha (ER{alpha}) signaling and a luminal phenotype in MCF-7 breast cancer cells. Mol Endocrinol 2009, 23:1215-1230. 10.1210/me.2009-0062, 19423651.
71. Thyrell L, Hjortsberg L, Arulampalam V, Panaretakis T, Uhles S, Dagnell M, Zhivotovsky B, Leibiger I, Grander D, Pokrovskaja K. Interferon alpha-induced apoptosis in tumor cells is mediated through the phosphoinositide 3-kinase/mammalian target of rapamycin signaling pathway. J Biol Chem 2004, 279:24152-24162. 10.1074/jbc.M312219200, 15056668.
72. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
73. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95:14863-14868. 10.1073/pnas.95.25.14863, 24541, 9843981.