Cross platform standardisation of an experimental pipeline for use in the identification of dysregulated human circulating MiRNAs

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Kelly, Helena ^a   Downing, Tim ^b   Tuite, Nina L ^a   Smith, Terry J ^a   Kerin, Michael J ^a   Dwyer, Róisín M ^a   Clancy, Eoin ^a   Barry, Thomas ^a   Reddington, Kate ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 320A; UNCLASSIFIED DRUG; RNA;

ADULT; AGED; ARTICLE; BREAST CANCER; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; MIDDLE AGED; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA ISOLATION; RNA PURIFICATION; RNA SEQUENCE; STANDARDIZATION; BLOOD; BREAST TUMOR; CASE CONTROL STUDY; COHORT ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; STANDARD;

BREAST NEOPLASMS; CASE-CONTROL STUDIES; COHORT STUDIES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MOLECULAR SEQUENCE ANNOTATION; REAL-TIME POLYMERASE CHAIN REACTION; REFERENCE STANDARDS; RNA, NEOPLASM; SEQUENCE ANALYSIS, RNA;

EID: 84944769133     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137389     Document Type: Article

References (83)

1. Grosshans H, FilipowiczW(2008) Molecular biology-The expanding world of small RNAs. Nature 451: 414-416. doi: 10.1038/451414a PMID: 18216846
2. Silahtaroglu A, Stenvang J (2010) MicroRNAs, epigenetics and disease. Essays in Biochemistry: Epigenetics, Disease and Behaviour 48: 165-185.
3. Ambros V (2004) The functions of animal microRNAs. Nature 431: 350-355. PMID: 15372042
4. Zhang BH, Pan XP, Cobb GP, Anderson TA (2006) Plant microRNA: A small regulatory molecule with big impact. Developmental Biology 289: 3-16. PMID: 16325172
5. Cullen BR (2006) Viruses and microRNAs. Nature Genetics 38: S25-S30. PMID: 16736021
6. Jiang Q, Wang Y, Hao Y, Juan L, Teng M, et al. (2009) miR2Disease: a manually curated database for microRNA deregulation in human disease. Nucleic Acids Research 37: D98-D104. doi: 10.1093/nar/ gkn714 PMID: 18927107
7. Martins PAD, Leptidis S, Salic K, De Windt LJ (2010) MicroRNA Regulation in Cardiovascular Disease. Current Drug Targets 11: 900-906. PMID: 20415652
8. Farazi TA, Spitzer JI, Morozov P, Tuschl T (2011) miRNAs in human cancer. Journal of Pathology 223: 102-115. doi: 10.1002/path.2806 PMID: 21125669
9. Saugstad JA (2010) MicroRNAs as effectors of brain function with roles in ischemia and injury, neuroprotection, and neurodegeneration. Journal of Cerebral Blood Flow and Metabolism 30: 1564-1576. doi: 10.1038/jcbfm.2010.101 PMID: 20606686
10. Schickel R, Boyerinas B, Park SM, Peter ME (2008) MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 27: 5959-5974. doi: 10.1038/onc.2008.274 PMID: 18836476
11. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian micro- RNA targets. Cell 115: 787-798. PMID: 14697198
12. Friedman RC, Farh KKH, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Research 19: 92-105. doi: 10.1101/gr.082701.108 PMID: 18955434
13. Zhang R, Su B (2009) Small but influential: the role of microRNAs on gene regulatory network and 3 ' UTR evolution. Journal of Genetics and Genomics 36: 1-6. doi: 10.1016/S1673-8527(09)60001-1 PMID: 19161940
14. Bartel DP, Chen CZ (2004) Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nature Reviews Genetics 5: 396-400. PMID: 15143321
15. Luo X, Burwinkel B, Tao S, Brenner H (2011) MicroRNA Signatures: Novel Biomarker for Colorectal Cancer? Cancer Epidemiology Biomarkers & Prevention 20: 1272-1286. doi: 10.1158/1055-9965. EPI-11-0035 PMID: 21551242
16. Kosaka N, Iguchi H, Ochiya T (2010) Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Science 101: 2087-2092. doi: 10.1111/j.1349-7006.2010. 01650.x PMID: 20624164
17. Roth C, Kasimir-Bauer S, Pantel K, Schwarzenbach H (2011) Screening for circulating nucleic acids and caspase activity in the peripheral blood as potential diagnostic tools in lung cancer. Molecular Oncology 5: 281-291. doi: 10.1016/j.molonc.2011.02.002 PMID: 21398193
18. Shapira I, Oswald M, Lovecchio J, Khalili H, Menzin A, et al. (2014) Circulating biomarkers for detection of ovarian cancer and predicting cancer outcomes. Br J Cancer 110: 976-983. doi: 10.1038/bjc.2013. 795 PMID: 24366298
19. Mar-Aguilar F, Mendoza-Ramírez JA, Malagón-Santiago I, Espino-Silva PK, Santuario-Facio SK, et al. (2013) Serum Circulating microRNA Profiling for Identification of Potential Breast Cancer Biomarkers. Disease Markers 34. doi: 10.3233/DMA-120957 PMID: 23334650
20. Chen CF, Ridzon DA, Broomer AJ, Zhou ZH, Lee DH, et al. (2005) Real-time quantification of micro- RNAs by stem-loop RT-PCR. Nucleic Acids Research 33. PMID: 16314309
21. Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39: 519-525. PMID: 16235564
22. Hanna JA, Wimberly H, Kumar S, Slack F, Agarwal S, et al. (2012) Quantitative analysis of microRNAs in tissue microarrays by in situ hybridization. Biotechniques 52: 235-+. doi: 10.2144/000113837 PMID: 22482439
23. Yin JQ, Zhao RC, Morris KV (2008) Profiling microRNA expression with microarrays. Trends in Biotechnology 26: 70-76. doi: 10.1016/j.tibtech.2007.11.007 PMID: 18191262
24. Li W, Ruan KC (2009) MicroRNA detection by microarray. Analytical and Bioanalytical Chemistry 394: 1117-1124. doi: 10.1007/s00216-008-2570-2 PMID: 19132354
25. Hafner M, Landgraf P, Ludwig J, Rice A, Ojo T, et al. (2008) Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 44: 3-12. PMID: 18158127
26. Lopez J, Diallo A, Cruceanu C, Fiori L, Laboissiere S, et al. (2015) Biomarker discovery: quantification of microRNAs and other small non-coding RNAs using next generation sequencing. BMC Medical Genomics 8: 35. doi: 10.1186/s12920-015-0109-x PMID: 26130076
27. Becker C, Hammerle-Fickinger A, Riedmaier I, Pfaffl MW(2010) mRNA and microRNA quality control for RT-qPCR analysis. Methods 50: 237-243. doi: 10.1016/j.ymeth.2010.01.010 PMID: 20079844
28. Benes V, Castoldi M (2010) Expression profiling of microRNA using real-time quantitative PCR, how to use it and what is available. Methods 50: 244-249. doi: 10.1016/j.ymeth.2010.01.026 PMID: 20109550
29. Pieter M, Nicole H, Lukas B, Ditte A, Nathalie B, et al. (2014) Evaluation of quantitative miRNA expression platforms in the microRNA quality control (miRQC) study. Nature Methods.
30. Chevillet JR, Lee I, Briggs HA, He Y, Wang K (2014) Issues and Prospects of microRNA-Based Biomarkers in Blood and Other Body Fluids. Molecules 19: 6080-6105. doi: 10.3390/molecules19056080 PMID: 24830712
31. Git A, Dvinge H, Salmon-Divon M, Osborne M, Kutter C, et al. (2010) Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression. Rna-a Publication of the Rna Society 16: 991-1006.
32. Moldovan L, Batte KE, Trgovcich J, Wisler J, Marsh CB, et al. (2014) Methodological challenges in utilizing miRNAs as circulating biomarkers. Journal of Cellular and Molecular Medicine 18: 371-390. doi: 10.1111/jcmm.12236 PMID: 24533657
33. Redshaw N, Wilkes T, Whale A, Cowen S, Huggett J, et al. (2013) A comparison of miRNA isolation and RT-qPCR technologies and their effects on quantification accuracy and repeatability. Biotechniques 54: 155-+. doi: 10.2144/000114002 PMID: 23477383
34. Huggett J, Dheda K, Bustin S, Zumla A (2005) Real-time RT-PCR normalisation; strategies and considerations. Genes Immun 6: 279-284. PMID: 15815687
35. Risso D, Ngai J, Speed TP, Dudoit S (2014) Normalization of RNA-seq data using factor analysis of control genes or samples. Nature Biotechnology 32: 896-902. doi: 10.1038/nbt.2931 PMID: 25150836
36. Kratz A, Carninci P (2014) The devil in the details of RNA-seq. Nat Biotech 32: 882-884.
37. Lu C, Meyers BC, Green PJ (2007) Construction of small RNA cDNA libraries for deep sequencing. Methods 43: 110-117. PMID: 17889797
38. http://www.preanalytix.com/product-catalog/blood/rna/products/paxgene-blood-rna-kit/.
39. Meyer M, Kircher M (2010) Illumina Sequencing Library Preparation for Highly Multiplexed Target Capture and Sequencing. Cold Spring Harb Protoc 2010.
40. Illumina http://www.illumina.com/applications/sequencing/rna.html.
41. Bentley D (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59. doi: 10.1038/nature07517 PMID: 18987734
42. www.bioinformatics.babraham.ac.uk/projects/fastqc/.
43. http://www.clcbio.com/.
44. Lawless N, Foroushani ABK, McCabe MS, O'Farrelly C, Lynn DJ (2013) Next Generation Sequencing Reveals the Expression of a Unique miRNA Profile in Response to a Gram-Positive Bacterial Infection. Plos One 8. doi: 10.1371/journal.pone.0057543 PMID: 23472090
45. Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5: 621-628. doi: 10.1038/nmeth.1226 PMID: 18516045
46. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology 11. doi: 10.1186/gb-2010-11-3-r25 PMID: 20196867
47. Bullard JH, Purdom E, Hansen KD, Dudoit S (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. Bmc Bioinformatics 11. doi: 10.1186/1471- 2105-11-94 PMID: 20167110
48. Garmire LX, Subramaniam S (2012) Evaluation of normalization methods in mammalian microRNASeq data. Rna-a Publication of the Rna Society 18: 1279-1288.
49. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193. PMID: 12538238
50. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140. doi: 10.1093/bioinformatics/ btp616 PMID: 19910308
51. Griffiths-Jones S, Grocock R, van Dongen S, Bateman A, Enright A (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34: D140-144. PMID: 16381832
52. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, et al. (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences 105: 10513-10518.
53. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Research 36: D154-D158. PMID: 17991681
54. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210. PMID: 11752295
55. Svec D, Tichopad A, Novosadova V, Pfaffl MW, Kubista M (2015) How good is a PCR efficiency estimate: Recommendations for precise and robust qPCR efficiency assessments. Biomolecular Detection and Quantification.
56. Kroh E, Parkin R, Mitchell P, Tewari M (2010) Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 50: 298-301. doi: 10. 1016/j.ymeth.2010.01.032 PMID: 20146939
57. McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A (2011) Analysis of Circulating MicroRNA: Preanalytical and Analytical Challenges. Clinical Chemistry 57: 833-840. doi: 10.1373/ clinchem.2010.157198 PMID: 21487102
58. Baker M (2010) MicroRNA profiling: separating signal from noise. Nature Methods 7: 687-692. doi: 10. 1038/nmeth0910-687 PMID: 20805796
59. Meyer CA, Liu XS (2014) Identifying and mitigating bias in next-generation sequencing methods for chromatin biology. Nature Reviews Genetics 15: 709-721. doi: 10.1038/nrg3788 PMID: 25223782
60. Patnaik SK, Yendamuri S, Kannisto E, Kucharczuk JC, Singhal S, et al. (2012) MicroRNA Expression Profiles of Whole Blood in Lung Adenocarcinoma. Plos One 7. doi: 10.1371/journal.pone.0046045 PMID: 23029380
61. Chal V, Vassilakos A, Lee Y, Wright JA, Young AH (2005) Optimization of the PAXgene (TM) blood RNA extraction system for gene expression analysis of clinical samples. Journal of Clinical Laboratory Analysis 19: 182-188. PMID: 16170815
62. Kim J-H, Jin H-O, Park J-A, Chang YH, Hong YJ, et al. (2014) Comparison of three different kits for extraction of high-quality RNA from frozen blood. SpringerPlus 3: 76. doi: 10.1186/2193-1801-3-76 PMID: 24567882
63. Keller A, Leidinger P, Steinmeyer F, Stähler C, Franke A, et al. (2014) Comprehensive analysis of microRNA profiles in multiple sclerosis including next-generation sequencing. Multiple Sclerosis Journal 20: 295-303. doi: 10.1177/1352458513496343 PMID: 23836875
64. Fleige S, Pfaffl M (2006) RNA integrity and the effect on the real-time qRT-PCR performance. Mol Aspects Med 27: 126-139. PMID: 16469371
65. Luo HE, Li JT, Chia BKH, Robson P, Nagarajan N (2014) The importance of study design for detecting differentially abundant features in high-throughput experiments. Genome Biology 15. doi: 10.1186/ s13059-014-0527-7 PMID: 25517037
66. Hicks SC, Irizarry RA (2014) When to use Quantile Normalization?
67. Zhou X, Oshlack A, Robinson MD (2013) miRNA-Seq normalization comparisons need improvement. Rna-a Publication of the Rna Society 19: 733-734.
68. Cheng ZA, Qiu SB, Jiang L, Zhang AL, Bao WJ, et al. (2013) MiR-320a is Downregulated in Patients with Myasthenia Gravis and Modulates Inflammatory Cytokines Production by Targeting Mitogen-activated Protein Kinase 1. Journal of Clinical Immunology 33: 567-576. doi: 10.1007/s10875-012-9834-5 PMID: 23196978
69. Shang C, Zhang H, Guo Y, Hong Y, Liu YH, et al. (2014) MiR-320a down-regulation mediates bladder carcinoma invasion by targeting ITGB3. Molecular Biology Reports 41: 2521-2527. doi: 10.1007/ s11033-014-3110-0 PMID: 24443232
70. Zhao H, Dong T, Zhou H, Wang L, Huang A, et al. (2013) miR-320a suppresses colorectal cancer progression by targeting Rac1. Carcinogenesis.
71. Sun J-Y, Huang Y, Li J-P, Zhang X, Wang L, et al. (2012) MicroRNA-320a suppresses human colon cancer cell proliferation by directly targeting β-catenin. Biochemical and Biophysical Research Communications 420: 787-792. doi: 10.1016/j.bbrc.2012.03.075 PMID: 22459450
72. Huang A, Zhao H, Quan Y, Jin R, Feng B, et al. (2014) E2A Predicts Prognosis of Colorectal Cancer Patients and Regulates Cancer Cell Growth by Targeting miR-320a. PLoS ONE 9: e85201. doi: 10. 1371/journal.pone.0085201 PMID: 24454819
73. Wu YY, Chen YL, Jao YC, Hsieh IS, Chang KC, et al. (2014) miR-320 regulates tumor angiogenesis driven by vascular endothelial cells in oral cancer by silencing neuropilin 1. Angiogenesis 17: 247-260. doi: 10.1007/s10456-013-9394-1 PMID: 24114198
74. Cheng C, Chen ZQ, Shi XT (2014) MicroRNA-320 inhibits osteosarcoma cells proliferation by directly targeting fatty acid synthase. Tumor Biology 35: 4177-4183. doi: 10.1007/s13277-013-1546-9 PMID: 24390663
75. Yang HP, Yu J, Wang L, Ding D, Zhang L, et al. (2014) miR-320a is an independent prognostic biomarker for invasive breast cancer. Oncology Letters 8: 1043-1050. PMID: 25120655
76. Li Q, Yao Y, Eades G, Liu Z, Zhang Y, et al. (2014) Downregulation of miR-140 promotes cancer stem cell formation in basal-like early stage breast cancer. Oncogene 33: 2589-2600. doi: 10.1038/onc. 2013.226 PMID: 23752191
77. Yuan YF, Shen YX, Xue L, Fan H (2013) miR-140 Suppresses Tumor Growth and Metastasis of Non- Small Cell Lung Cancer by Targeting Insulin-Like Growth Factor 1 Receptor. Plos One 8. doi: 10.1371/ journal.pone.0073604 PMID: 24039995
78. Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Newell J, et al. (2010) Circulating microRNAs as Novel Minimally Invasive Biomarkers for Breast Cancer. Annals of Surgery 251: 499-505 410.1097/ SLA.1090b1013e3181cc1939f. doi: 10.1097/SLA.0b013e3181cc939f PMID: 20134314
79. Su ZQ, Labaj PP, Li S, Thierry-Mieg J, Thierry-Mieg D, et al. (2014) A comprehensive assessment of RNA-seq accuracy, reproducibility and information content by the Sequencing Quality Control Consortium. Nature Biotechnology 32: 903-914. doi: 10.1038/nbt.2957 PMID: 25150838
80. Aird D, Ross MG, Chen WS, Danielsson M, Fennell T, et al. (2011) Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries. Genome Biology 12. doi: 10.1186/gb-2011-12-2-r18 PMID: 21338519
81. Kim Y, Yeo J, Kim B, Ha M, Kim V (2012) Short Structured RNAs with Low GC Content Are Selectively Lost during Extraction from a Small Number of Cells. Mol Cell 46: 893-895. doi: 10.1016/j.molcel. 2012.05.036 PMID: 22749402
82. VanGuilder HD, Vrana KE, FreemanWM(2008) Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques 44: 619-626. doi: 10.2144/000112776 PMID: 18474036
83. Leidner RS, Li L, Thompson CL (2013) Dampening Enthusiasm for Circulating MicroRNA in Breast Cancer. PLoS ONE 8. doi: 10.1371/journal.pone.0057841 PMID: 23472110