Data normalization strategies for microRNA quantification

Clinical Chemistry

Volumn 61, Issue 11, 2015, Pages 1333-1342

  Schwarzenbach, Heidi ^a   Da Silva, Andreia Machado ^b,c,d   Calin, George ^b   Pantel, Klaus ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF PORTO   (Portugal)

^d INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 16; SMALL NUCLEAR RNA;

3' UNTRANSLATED REGION; BODY FLUID; CELL SURVIVAL; DATA NORMALIZATION; DATA PROCESSING; EXOSOME; HUMAN; NORTHERN BLOTTING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; REVIEW; RNA ANALYSIS; RNA DEGRADATION; SIZE EXCLUSION CHROMATOGRAPHY; ULTRACENTRIFUGATION; ANIMAL; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; PROCEDURES; REPRODUCIBILITY; STANDARD; STANDARDS; WORKFLOW;

ANIMALS; GENE EXPRESSION PROFILING; HUMANS; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REFERENCE STANDARDS; REPRODUCIBILITY OF RESULTS; WORKFLOW;

EID: 84946576277     PISSN: 00099147     EISSN: 15308561     Source Type: Journal    
DOI: 10.1373/clinchem.2015.239459     Document Type: Review

References (86)

1. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 2014;15: 509-24.
2. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004;116: 281-97.
3. Calin GA, Croce CM. MicroRNA-cancer connection: The beginning of a new tale. Cancer Res 2006;66: 7390-4.
4. ArdekaniAM, NaeiniMM.The role of microRNAs inhuman diseases. Avicenna J Med Biotechnol 2010;2: 161-79.
5. Schwarzenbach H, Nishida N, Calin GA, Pantel K. Clinical relevance of circulating cell-free microRNAs in cancer. Nat Rev Clin Oncol 2014;11: 145-56.
6. van Schooneveld E, Wildiers H, Vergote I, Vermeulen PB, Dirix LY, Van Laere SJ. Dysregulation of microRNAs in breast cancer and their potential role as prognostic and predictive biomarkers in patient management. Breast Cancer Res 2015;17: 21.
7. Chen X, Liang H, Zhang J, Zen K, Zhang CY. Horizontal transfer of microRNAs: Molecular mechanisms and clinical applications. Protein Cell 2012;3: 28-37.
8. Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: Biomarkers, functions and therapy. Trends Mol Med 2014;20: 460-9.
9. Moreno-Moya JM, Vilella F, Simon C. MicroRNA: Key gene expression regulators. Fertil Steril 2014;101: 1516-23.
10. Tiberio P, Callari M, Angeloni V, Daidone MG, Appierto V. Challenges in using circulating miRNAs as cancer biomarkers. Biomed Res Int 2015;2015: 731479.
11. Biassoni R, Raso A, editors. MiRNA and microRNA purity and integrity: The key to success in expression profiling. New York: Springer; 2014.
12. Li J, Smyth P, Flavin R, Cahill S, Denning K, Aherne S, et al. Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalinfixed paraffin-embedded (FFPE) cells and snap frozen cells. BMC Biotechnol 2007;7: 36.
13. Monleau M, Bonnel S, Gostan T, Blanchard D, Courgnaud V, Lecellier CH. Comparison of different extraction techniques to profile microRNAs from human sera and peripheral blood mononuclear cells. BMC Genomics 2014;15: 395.
14. Glynn CL, Khan S, Kerin MJ, Dwyer RM. Isolation of secreted microRNAs (miRNAs) from cell-conditioned media. MicroRNA 2013;2: 14-9.
15. Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, et al. The microRNA spectrum in 12 body fluids. Clin Chem 2010;56: 1733-41.
16. Rani S. MicroRNA profiling of exosomes isolated from biofluids and conditioned media. Methods Mol Biol 2014;1182: 131-44.
17. Ibberson D, Benes V, Muckenthaler MU, Castoldi M. RNA degradation compromises the reliability of microRNA expression profiling. BMC Biotechnol 2009;9: 102.
18. Kim DJ, Linnstaedt S, Palma J, Park JC, Ntrivalas E, Kwak-Kim JY, et al. Plasma components affect accuracy of circulating cancer-related microRNA quantitation. J Mol Diagn 2012;14: 71-80.
19. Farina NH, Wood ME, Perrapato SD, Francklyn CS, Stein GS, Stein JL, Lian JB. Standardizing analysis of circulating microRNA: Clinical and biological relevance. J Cell Biochem 2014;115: 805-11.
20. MacLellan SA, MacAulay C, Lam S, Garnis C. Preprofiling factors influencing serum microRNA levels. BMC Clin Pathol 2014;14: 27.
21. Witwer KW, Buzas EI, Bemis LT, Bora A, Lasser C, Lotvall J, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013;2.
22. Liu R, Chen X, Du Y, Yao W, Shen L, Wang C, et al. Serum microRNA expression profile as a biomarker in the diagnosis and prognosis of pancreatic cancer. Clin Chem 2012;58: 610-8.
23. Vasilescu C, Rossi S, Shimizu M, Tudor S, Veronese A, Ferracin M, et al. MicroRNA fingerprints identify miR-150 as a plasma prognostic marker in patients with sepsis. PLoS One 2009;4: E7405.
24. Aushev VN, Zborovskaya IB, Laktionov KK, Girard N, Cros MP, Herceg Z, Krutovskikh V. Comparisons of microRNA patterns in plasma before and after tumor removal reveal new biomarkers of lung squamous cell carcinoma. PLoS One 2013;8: E78649.
25. Fang L, Li H, Wang L, Hu J, Jin T, Wang J, Yang BB. MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget 2014;5: 2974-87.
26. Oksvold MP, Kullmann A, Forfang L, Kierulf B, Li M, Brech A, et al. Expression of B-cell surface antigens in subpopulations of exosomes released from B-cell lymphoma cells. Clin Ther 2014;36: 847-62 e1.
27. Boing AN, van der Pol E, Grootemaat AE, Coumans FA, Sturk A, Nieuwland R. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles 2014;3.
28. Mathivanan S, Lim JW, Tauro BJ, Ji H, Moritz RL, Simpson RJ. Proteomics analysis of A33 immunoaffinitypurified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol Cell Proteomics 2010;9: 197-208.
29. Witwer KW. Circulating microRNA biomarker studies: Pitfalls and potential solutions. Clin Chem 2015; 61: 56-63.
30. Haider BA, Baras AS, McCall MN, Hertel JA, Cornish TC, Halushka MK. A critical evaluation of microRNA biomarkers in non-neoplastic disease. PLoS One 2014;9: E89565.
31. Benes V, Castoldi M. Expression profiling of microRNA using real-time quantitative PCR, how to use it and what is available. Methods 2010;50: 244-9.
32. Thomson JM, Parker JS, Hammond SM. Microarray analysis of miRNA gene expression. Methods Enzymol 2007;427: 107-22.
33. Sato F, Tsuchiya S, Terasawa K, Tsujimoto G. Intra-platform repeatability and inter-platform comparability of microRNA microarray technology. PLoS One 2009;4: E5540.
34. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, Speleman F, Vandesompele J. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol 2009;10: R64.
35. Meyer SU, Pfaffl MW, Ulbrich SE. Normalization strategies for microRNA profiling experiments: A 'normal' way to a hidden layer of complexity? Biotechnol Lett 2010;32: 1777-88.
36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta c(t)) method. Methods 2001;25: 402-8.
37. Rai SN, Ray HE, Yuan X, Pan J, Hamid T, Prabhu SD. Statistical analysis of repeated microRNA highthroughput data with application to human heart failure: A review of methodology. Open AccessMedStat 2012;2012: 21-31.
38. Bustin SA, Beaulieu JF, Huggett J, Jaggi R, Kibenge FS, Olsvik PA, et al. MIQE precis: Practical implementation of minimum standard guidelines for fluorescencebased quantitative real-time PCR experiments. BMC Mol Biol 2010;11: 74.
39. Chugh P, Dittmer DP. Potential pitfalls in microRNA profiling. Wiley Interdiscip Rev RNA 2012;3: 601-16.
40. Yan W, Li R, Liu Y, Yang P, Wang Z, Zhang C, et al. MicroRNA expression patterns in the malignant progression of gliomas and a 5-microRNA signature for prognosis. Oncotarget 2014;5: 12908-15.
41. Yau TO, Wu CW, Dong Y, Tang CM, Ng SS, Chan FK, et al. MicroRNA-221 and microRNA-18a identification in stool as potential biomarkers for the non-invasive diagnosis of colorectal carcinoma. Br J Cancer 2014;111: 1765-71.
42. Liu WJ, Xu Q, Sun LP, Dong QG, He CY, Yuan Y. Expression of serum let-7c, let-7i, and let-7f microRNA with its target gene, pepsinogen C, in gastric cancer and precancerous disease. Tumour Biol 2015;36: 3337-43.
43. Wang J, Pei Y, Zhong Y, Jiang S, Shao J, Gong J. Altered serum microRNAs as novel diagnostic biomarkers for atypical coronary artery disease. PLoS One 2014;9: E107012.
44. Kuhlmann JD, Baraniskin A, Hahn SA, Mosel F, Bredemeier M, Wimberger P, et al. Circulating U2 small nuclear RNA fragments as a novel diagnostic tool for patients with epithelial ovarian cancer. Clin Chem 2014;60: 206-13.
45. Spiekermann M, Dieckmann KP, Balks T, Bullerdiek J, Belge G. Is relative quantification dispensable for the measurement of microRNAs as serum biomarkers in germ cell tumors? Anticancer Res 2015;35: 117-21.
46. Wang X, Gardiner EJ, Cairns MJ. Optimal consistency in microRNA expression analysis using reference-genebased normalization. Mol Biosyst 2015;11: 1235-40.
47. Serafin A, Foco L, Blankenburg H, Picard A, Zanigni S, Zanon A, et al. Identification of a set of endogenous reference genes for miRNA expression studies in Parkinson's disease blood samples. BMC Res Notes 2014;7: 715.
48. Roth C, Rack B, Muller V, Janni W, Pantel K, Schwarzenbach H. Circulating microRNAs as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res 2010;12: R90.
49. Mahdipour M, Van Tol HT, Stout TA, Roelen BA. 225 validation of reference microRNAs for normalizing expression data generated by quantitative PCR. Reprod Fertil Dev 2014;27: 202.
50. Song J, Bai Z, Han W, Zhang J, Meng H, Bi J, et al. Identification of suitable reference genes for qPCR analysis of serum microRNA in gastric cancer patients. Dig Dis Sci 2012;57: 897-904.
51. Shen Y, Tian F, Chen Z, Li R, Ge Q, Lu Z. Amplificationbased method for microRNA detection. Biosens Bioelectron 2015;71: 322-31.
52. Benz F, Roderburg C, Vargas Cardenas D, Vucur M, Gautheron J, Koch A, et al. U6 is unsuitable for normalization of serum miRNA levels in patients with sepsis or liver fibrosis. Exp Mol Med 2013;45: E42.
53. Gee HE, Buffa FM, Camps C, Ramachandran A, Leek R, Taylor M, et al. The small-nucleolar RNAs commonly used for microRNA normalisation correlate with tumour pathology and prognosis. Br J Cancer 2011;104: 1168-77.
54. Xiang M, Zeng Y, Yang R, Xu H, Chen Z, Zhong J, et al. U6 is not a suitable endogenous control for the quantification of circulating microRNAs. Biochem Biophys Res Commun 2014;454: 210-4.
55. Lamba V, Ghodke-Puranik Y, Guan W, Lamba JK. Identification of suitable reference genes for hepatic microRNA quantitation. BMC Res Notes 2014;7: 129.
56. Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004;64: 5245-50.
57. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002;3: RESEARCH0034.
58. Ratert N, Meyer HA, Jung M, Mollenkopf HJ, Wagner I, Miller K, et al. Reference miRNAs for miRNAome analysis of urothelial carcinomas. PLoS One 2012;7: E39309.
59. Wotschofsky Z, Meyer HA, Jung M, Fendler A, Wagner I, Stephan C, et al. Reference genes for the relative quantification of microRNAs in renal cell carcinomas and their metastases. Anal Biochem 2011;417: 233-41.
60. Torres A, Torres K, Wdowiak P, Paszkowski T, Maciejewski R. Selection and validation of endogenous controls for microRNA expression studies in endometrioid endometrial cancer tissues. Gynecol Oncol 2013;130: 588-94.
61. Han HS, Jo YN, Lee JY, Choi SY, Jeong Y, Yun J, Lee OJ. Identification of suitable reference genes for the relative quantification of microRNAs in pleural effusion. Oncol Lett 2014;8: 1889-95.
62. Muller V, Gade S, Steinbach B, Loibl S, von Minckwitz G, Untch M, et al. Changes in serum levels of miR-21, miR-210, and miR-373 in HER2-positive breast cancer patients undergoing neoadjuvant therapy: A translational research project within the Geparquinto trial. Breast Cancer Res Treat 2014;147: 61-8.
63. McDermott AM, Kerin MJ, Miller N. Identification and validation of miRNAs as endogenous controls for RQPCR in blood specimens for breast cancer studies. PLoS One 2013;8: E83718.
64. Schaefer A, Jung M, Miller K, Lein M, Kristiansen G, Erbersdobler A, Jung K. Suitable reference genes for relative quantification of miRNA expression in prostate cancer. Exp Mol Med 2010;42: 749-58.
65. Delfino KR, Rodriguez-Zas SL. Transcription factormicroRNA-target gene networks associated with ovarian cancer survival and recurrence. PLoS One 2013; 8: E58608.
66. Ell B, Mercatali L, Ibrahim T, Campbell N, Schwarzenbach H, Pantel K, et al. Tumor-induced osteoclast miRNA changes as regulators and biomarkers of osteolytic bone metastasis. Cancer Cell 2013;24: 542-56.
67. Hu Z, Dong J, Wang LE, MaH, Liu J, Zhao Y, et al. Serum microRNA profiling and breast cancer risk: The use of mir-484/191 as endogenous controls. Carcinogenesis 2012;33: 828-34.
68. Liu J, Gao J, Du Y, Li Z, Ren Y, Gu J, et al. Combination of plasma microRNAs with serum CA19-9 for early detection of pancreatic cancer. Int J Cancer 2012;131: 683-91.
69. Xiao G, Tang H, Wei W, Li J, Ji L, Ge J. Aberrant expression of microRNA-15a and microRNA-16 synergistically associates with tumor progression and prognosis in patients with colorectal cancer. Gastroenterol Res Pract 2014: 364549, 2014.
70. Zuo Z, Calin GA, de Paula HM, Medeiros LJ, Fernandez MH, Shimizu M, et al. Circulating microRNAs let-7a and miR-16 predict progression-free survival and overall survival in patients with myelodysplastic syndrome. Blood 2011;118: 413-5.
71. Peltier HJ, Latham GJ. Normalization of microRNA expression levels in quantitative RT-PCR assays: Identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 2008;14: 844-52.
72. Hu J, Wang Z, Liao BY, Yu L, Gao X, Lu S, et al. Human miR-1228 as a stable endogenous control for the quantification of circulating microRNAs in cancer patients. Int J Cancer 2014;135: 1187-94.
73. Zhu HT, Dong QZ, Wang G, Zhou HJ, Ren N, Jia HL, et al. Identification of suitable reference genes for qRT-PCR analysis of circulating microRNAs in hepatitis B virusinfected patients. Mol Biotechnol 2012;50: 49-56.
74. Sanders I, Holdenrieder S, Walgenbach-Brunagel G, von Ruecker A, Kristiansen G, Muller SC, Ellinger J. Evaluation of reference genes for the analysis of serum miRNA in patients with prostate cancer, bladder cancer and renal cell carcinoma. Int J Urol 2012;19: 1017-25.
75. Shen Y, Li Y, Ye F, Wang F, Wan X, Lu W, Xie X. Identification of miR-23a as a novel microRNA normalizer for relative quantification in human uterine cervical tissues. Exp Mol Med 2011;43: 358-66.
76. Tang G, Shen X, Lv K, Wu Y, Bi J, Shen Q. Different normalization strategies might cause inconsistent variation in circulating microRNAs in patients with hepatocellular carcinoma. Med Sci Monit 2015;21: 617-24.
77. Wang L, Liu Y, Du L, Li J, Jiang X, Zheng G, et al. Identification and validation of reference genes for the detection of serum microRNAs by reverse transcriptionquantitative polymerase chain reaction in patients with bladder cancer. Mol Med Rep 2015;12: 615-22.
78. Li Y, Zhang L, Liu F, Xiang G, Jiang D, Pu X. Identification of endogenous controls for analyzing serum exosomal miRNA in patients with hepatitis B or hepatocellular carcinoma. Dis Markers 2015: 893594, 2015.
79. Wang P, Yang D, Zhang H, Wei X, Ma T, Cheng Z, et al. Early detection of lung cancer in serum by a panel of microRNA biomarkers. Clin Lung Cancer 2014;16: 313-9.e1.
80. Dong BL, Wang Z, Zhang Z, Wang J. Clinical significance of microRNA-24 expression in esophageal squamous cell carcinoma. Neoplasma 2015;62: 250-8.
81. Xu T, Liao Z, O'Reilly MS, Levy LB, Welsh JW, Wang LE, et al. Serum inflammatory miRNAs predict radiation esophagitis in patients receiving definitive radiochemotherapy for non-small cell lung cancer. Radiother Oncol 2014;113: 379-84.
82. Liu M, Liu J, Wang L, Wu H, Zhou C, Zhu H, et al. Association of serum microRNA expression in hepatocellular carcinomas treated with transarterial chemoembolization and patient survival. PLoS One 2014;9: E109347.
83. Anadol E, Schierwagen R, Elfimova N, Tack K, Schwarze-Zander C, Eischeid H, et al. Circulating microRNAs as a marker for liver injury in human immunodeficiency virus patients. Hepatology 2015;61: 46-55.
84. Becker C, Hammerle-Fickinger A, Riedmaier I, Pfaffl MW. MiRNA and microRNA quality control for RT-qPCR analysis. Methods 2010;50: 237-43.
85. Sourvinou IS, Markou A, Lianidou ES. Quantification of circulating miRNAs in plasma: Effect of preanalytical and analytical parameters on their isolation and stability. J Mol Diagn 2013;15: 827-34.
86. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, et al. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009;55: 611-22.