Ultra-high throughput sequencing-based small RNA discovery and discrete statistical biomarker analysis in a collection of cervical tumours and matched controls

BMC Biology

Volumn 8, Issue , 2010, Pages

  Witten, Daniela ^a   Tibshirani, Robert ^a   Gu, Sam G ^b   Fire, Andrew ^b   Lui, Weng Onn ^b,c  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; MICRORNA;

ARTICLE; BIOLOGY; CLUSTER ANALYSIS; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE LIBRARY; GENETICS; METHODOLOGY; STATISTICAL MODEL;

CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE LIBRARY; LINEAR MODELS; MICRORNAS; SEQUENCE ANALYSIS, DNA;

EID: 77951953494     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-8-58     Document Type: Article

References (77)

1. Hamilton AJ, Baulcombe DC. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 1999, 286:950-952. 10.1126/science.286.5441.950, 10542148.
2. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854. 10.1016/0092-8674(93)90529-Y, 8252621.
3. Birchler JA, Kavi HH. Molecular biology. Slicing and dicing for small RNAs. Science 2008, 320:1023-1024. 10.1126/science.1159018, 18467555.
4. Chapman EJ, Carrington JC. Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 2007, 8:884-896. 10.1038/nrg2179, 17943195.
5. Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 2008, 9:219-230. 10.1038/nrm2347, 18270516.
6. miRBase. , http://microrna.sanger.ac.uk/
7. Johnston RJ, Hobert O. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 2003, 426:845-849. 10.1038/nature02255, 14685240.
8. 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.
9. Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862. 10.1016/0092-8674(93)90530-4, 8252622.
10. 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, 113:25-36. 10.1016/S0092-8674(03)00231-9, 12679032.
11. 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, 13:790-795. 10.1016/S0960-9822(03)00250-1, 12725740.
12. Hoth S, Morgante M, Sanchez JP, Hanafey MK, Tingey SV, Chua NH. Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci 2002, 115:4891-4900. 10.1242/jcs.00175, 12432076.
13. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858. 10.1126/science.1064921, 11679670.
14. Lau NC, Lim LP, Weinstein EG, Bartel DP. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001, 294:858-862. 10.1126/science.1065062, 11679671.
15. Lee RC, Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001, 294:862-864. 10.1126/science.1065329, 11679672.
16. Blow MJ, Grocock RJ, van Dongen S, Enright AJ, Dicks E, Futreal PA, Wooster R, Stratton MR. RNA editing of human microRNAs. Genome Biol 2006, 7:R27. 1557993, 16594986, 10.1186/gb-2006-7-4-r27.
17. Habig JW, Dale T, Bass BL. miRNA editing--we should have inosine this coming. Mol Cell 2007, 25:792-793. 2583401, 17386255, 10.1016/j.molcel.2007.03.010.
18. Kawahara Y, Zinshteyn B, Sethupathy P, Iizasa H, Hatzigeorgiou AG, Nishikura K. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 2007, 315:1137-1140. 10.1126/science.1138050, 17322061.
19. Azuma-Mukai A, Oguri H, Mituyama T, Qian ZR, Asai K, Siomi H, Siomi MC. Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc Natl Acad Sci USA 2008, 105:7964-7969. 2430345, 18524951, 10.1073/pnas.0800334105.
20. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007, 129:1401-1414. 2681231, 17604727, 10.1016/j.cell.2007.04.040.
21. Wu H, Neilson JR, Kumar P, Manocha M, Shankar P, Sharp PA, Manjunath N. miRNA profiling of naive, effector and memory CD8 T cells. PLoS ONE 2007, 2:e1020. 2000354, 17925868, 10.1371/journal.pone.0001020.
22. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006, 442:203-207.
23. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, Perrimon N, Kellis M, Wohlschlegel JA, Sachidanandam R, et al. An endogenous small interfering RNA pathway in Drosophila. Nature 2008, 453:798-802. 10.1038/nature07007, 18463631.
24. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
25. Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML. A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 2008, 18:957-964. 2413163, 18469162, 10.1101/gr.074740.107.
26. Kawamura Y, Saito K, Kin T, Ono Y, Asai K, Sunohara T, Okada TN, Siomi MC, Siomi H. Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 2008, 453:793-797. 10.1038/nature06938, 18463636.
27. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE. Characterization of the piRNA complex from rat testes. Science 2006, 313:363-367. 10.1126/science.1130164, 16778019.
28. Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, Zhao Y, McDonald H, Zeng T, Hirst M, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 2008, 18:610-621. 2279248, 18285502, 10.1101/gr.7179508.
29. Okamura K, Chung WJ, Ruby JG, Guo H, Bartel DP, Lai EC. The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 2008, 453:803-806. 2735555, 18463630, 10.1038/nature07015.
30. Pak J, Fire A. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 2007, 315:241-244. 10.1126/science.1132839, 17124291.
31. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453:539-543. 10.1038/nature06908, 18404146.
32. Lui WO, Pourmand N, Patterson BK, Fire A. Patterns of known and novel small RNAs in human cervical cancer. Cancer Res 2007, 67:6031-6043. 10.1158/0008-5472.CAN-06-0561, 17616659.
33. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Mol Cell 2007, 28:328-336. 2763384, 17964270, 10.1016/j.molcel.2007.09.028.
34. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007, 130:89-100. 2729315, 17599402, 10.1016/j.cell.2007.06.028.
35. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature 2007, 448:83-86. 2475599, 17589500, 10.1038/nature05983.
36. Scheffer GL, Wijngaard PL, Flens MJ, Izquierdo MA, Slovak ML, Pinedo HM, Meijer CJ, Clevers HC, Scheper RJ. The drug resistance-related protein LRP is the human major vault protein. Nat Med 1995, 1:578-582. 10.1038/nm0695-578, 7585126.
37. Berninger P, Gaidatzis D, van Nimwegen E, Zavolan M. Computational analysis of small RNA cloning data. Methods 2008, 44:13-21. 10.1016/j.ymeth.2007.10.002, 18158128.
38. Tibshirani R, Hastie T, Narasimhan B, Chu G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci USA 2002, 99:6567-6572. 124443, 12011421, 10.1073/pnas.082099299.
39. Kuchenbauer F, Morin RD, Argiropoulos B, Petriv OI, Griffith M, Heuser M, Yung E, Piper J, Delaney A, Prabhu AL, et al. In-depth characterization of the microRNA transcriptome in a leukemia progression model. Genome Res 2008, 18:1787-1797. 2577858, 18849523, 10.1101/gr.077578.108.
40. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide. Cell 2008, 133:116-127. 10.1016/j.cell.2008.02.034, 18342361.
41. Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y. The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 2008, 49:493-500. 10.1093/pcp/pcn043, 18344228.
42. Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, Lai EC. The regulatory activity of microRNA* species has substantial influence on microRNA and 3' UTR evolution. Nat Struct Mol Biol 2008, 15:354-363. 2698667, 18376413, 10.1038/nsmb.1409.
43. Bender W. MicroRNAs in the Drosophila bithorax complex. Genes Dev 2008, 22:14-19. 2151010, 18172161, 10.1101/gad.1614208.
44. Stark A, Bushati N, Jan CH, Kheradpour P, Hodges E, Brennecke J, Bartel DP, Cohen SM, Kellis M. A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands. Genes Dev 2008, 22:8-13. 2151017, 18172160, 10.1101/gad.1613108.
45. Tyler DM, Okamura K, Chung WJ, Hagen JW, Berezikov E, Hannon GJ, Lai EC. Functionally distinct regulatory RNAs generated by bidirectional transcription and processing of microRNA loci. Genes Dev 2008, 22:26-36. 2151012, 18172163, 10.1101/gad.1615208.
46. Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S, Rajewsky N. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 2008, 26:407-415. 10.1038/nbt1394, 18392026.
47. Martinez I, Gardiner AS, Board KF, Monzon FA, Edwards RP, Khan SA. Human papillomavirus type 16 reduces the expression of microRNA-218 in cervical carcinoma cells. Oncogene 2008, 27:2575-2582. 2447163, 17998940, 10.1038/sj.onc.1210919.
48. Wang X, Tang S, Le SY, Lu R, Rader JS, Meyers C, Zheng ZM. Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth. PLoS ONE 2008, 3:e2557. 2438475, 18596939, 10.1371/journal.pone.0002557.
49. Chen HC, Chen GH, Chen YH, Liao WL, Liu CY, Chang KP, Chang YS, Chen SJ. MicroRNA deregulation and pathway alterations in nasopharyngeal carcinoma. Br J Cancer 2009, 100:1002-1011. 2661776, 19293812, 10.1038/sj.bjc.6604948.
50. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005, 65:7065-7070. 10.1158/0008-5472.CAN-05-1783, 16103053.
51. Michael MZ, O'Connor SM, van Holst Pellekaan NG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 2003, 1:882-891.
52. Chung TK, Cheung TH, Huen NY, Wong KW, Lo KW, Yim SF, Siu NS, Wong YM, Tsang PT, Pang MW, et al. Dysregulated microRNAs and their predicted targets associated with endometrioid endometrial adenocarcinoma in Hong Kong women. Int J Cancer 2009, 124:1358-1365. 10.1002/ijc.24071, 19065659.
53. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, et al. MicroRNA signatures in human ovarian cancer. Cancer Res 2007, 67:8699-8707. 10.1158/0008-5472.CAN-07-1936, 17875710.
54. Gottardo F, Liu CG, Ferracin M, Calin GA, Fassan M, Bassi P, Sevignani C, Byrne D, Negrini M, Pagano F, et al. Micro-RNA profiling in kidney and bladder cancers. Urol Oncol 2007, 25:387-392.
55. Fletcher AM, Heaford AC, Trask DK. Detection of metastatic head and neck squamous cell carcinoma using the relative expression of tissue-specific mir-205. Transl Oncol 2008, 1:202-208. 2582169, 19043531.
56. Markou A, Tsaroucha EG, Kaklamanis L, Fotinou M, Georgoulias V, Lianidou ES. Prognostic value of mature microRNA-21 and microRNA-205 overexpression in non-small cell lung cancer by quantitative real-time RT-PCR. Clin Chem 2008, 54:1696-1704. 10.1373/clinchem.2007.101741, 18719201.
57. Yu J, Ryan DG, Getsios S, Oliveira-Fernandes M, Fatima A, Lavker RM. MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proc Natl Acad Sci USA 2008, 105:19300-19305. 2587229, 19033458, 10.1073/pnas.0803992105.
58. Heselmeyer K, Schrock E, du Manoir S, Blegen H, Shah K, Steinbeck R, Auer G, Ried T. Gain of chromosome 3q defines the transition from severe dysplasia to invasive carcinoma of the uterine cervix. Proc Natl Acad Sci USA 1996, 93:479-484. 40262, 8552665, 10.1073/pnas.93.1.479.
59. Narayan G, Bourdon V, Chaganti S, Arias-Pulido H, Nandula SV, Rao PH, Gissmann L, Durst M, Schneider A, Pothuri B, et al. Gene dosage alterations revealed by cDNA microarray analysis in cervical cancer: identification of candidate amplified and overexpressed genes. Genes Chromosomes Cancer 2007, 46:373-384. 10.1002/gcc.20418, 17243165.
60. Yang YC, Shyong WY, Chang MS, Chen YJ, Lin CH, Huang ZD, Wang, Hsu MT, Chen ML. Frequent gain of copy number on the long arm of chromosome 3 in human cervical adenocarcinoma. Cancer Genet Cytogenet 2001, 131:48-53. 10.1016/S0165-4608(01)00510-6, 11734318.
61. Baskerville S, Bartel DP. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 2005, 11:241-247. 1370713, 15701730, 10.1261/rna.7240905.
62. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH, Hur K, Yoo MW, Lee HJ, Yang HK, et al. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res 2009, 37:1672-1681. 2655672, 19153141, 10.1093/nar/gkp002.
63. Lu M, Zhang Q, Deng M, Miao J, Guo Y, Gao W, Cui Q. An analysis of human microRNA and disease associations. PLoS One 2008, 3:e3420. 2559869, 18923704, 10.1371/journal.pone.0003420.
64. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, Goodall GJ. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 2008, 68:7846-7854. 10.1158/0008-5472.CAN-08-1942, 18829540.
65. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008, 9:582-589. 2396950, 18483486, 10.1038/embor.2008.74.
66. 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, 10:593-601. 10.1038/ncb1722, 18376396.
67. Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008, 283:14910-14914. 10.1074/jbc.C800074200, 18411277.
68. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008, 22:894-907. 2279201, 18381893, 10.1101/gad.1640608.
69. Wyman SK, Parkin RK, Mitchell PS, Fritz BR, O'Briant K, Godwin AK, Urban N, Drescher CW, Knudsen BS, Tewari M. Repertoire of microRNAs in epithelial ovarian cancer as determined by next generation sequencing of small RNA cDNA libraries. PLoS One 2009, 4:e5311. 2668797, 19390579, 10.1371/journal.pone.0005311.
70. Lee JW, Choi CH, Choi JJ, Park YA, Kim SJ, Hwang SY, Kim WY, Kim TJ, Lee JH, Kim BG, et al. Altered MicroRNA expression in cervical carcinomas. Clin Cancer Res 2008, 14:2535-2542. 10.1158/1078-0432.CCR-07-1231, 18451214.
71. Kickhoefer VA, Emre N, Stephen AG, Poderycki MJ, Rome LH. Identification of conserved vault RNA expression elements and a non-expressed mouse vault RNA gene. Gene 2003, 309:65-70. 10.1016/S0378-1119(03)00507-9, 12758122.
72. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grasser FA, van Dyk LF, Ho CK, Shuman S, Chien M, et al. Identification of microRNAs of the herpesvirus family. Nat Methods 2005, 2:269-276. 10.1038/nmeth746, 15782219.
73. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006, 13:1097-1101. 10.1038/nsmb1167, 17099701.
74. BLAST. , http://www.ncbi.nlm.nih.gov/blast/
75. BLAT. , http://genome.ucsc.edu
76. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415. 169194, 12824337, 10.1093/nar/gkg595.
77. The Comprehensive R Archive Network. , http://cran.r-project.org/