Fol. Biol. 2015, 61, 203-218

https://doi.org/10.14712/fb2015061060203

Circulating MicroRNAs: Methodological Aspects in Detection of These Biomarkers

A. Hruštincová, H. Votavová, Michaela Dostálová Merkerová

Department of Genomics, Institute of Hematology and Blood Transfusion, Prague, Czech Republic

Received April 2015
Accepted September 2015

References

1. Arroyoa, J. D., Chevillet, J. R., Kroh, E. M., Ruf, I. K., Pritchard, C. C., Gibson, D. F., Mitchell, P. S., Bennett, C. F., Pogosova-Agadjanyan, E. L., Stirewalt, D. L., Tait, J. F., Tewari, M. (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA 108, 5003-5008. <https://doi.org/10.1073/pnas.1019055108>
2. Baker, M. (2010) MicroRNA profiling: separating signal from noise. Nat. Methods 7, 687-692. <https://doi.org/10.1038/nmeth0910-687>
3. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297. <https://doi.org/10.1016/S0092-8674(04)00045-5>
4. Barupal, J. K., Saini, A. K., Chand, T., Meena, A., Beniwal, S., Suthar, J. R., Meena, N., Kachhwaha, S., Kothari, S. L. (2015) ExcellmiRDB for translational genomics: a curated online resource for extracellular microRNAs. OMICS 19, 24-30. <https://doi.org/10.1089/omi.2014.0106>
5. Benes, V., Castoldi, M. (2010) Expression profiling of micro- RNA using real-time quantitative PCR, how to use it and what is available. Methods 50, 244-249. <https://doi.org/10.1016/j.ymeth.2010.01.026>
6. Blenkiron, C., Askelund, K. J., Shanbhag, S. T., Chakraborty, M., Petrov, M. S., Delahunt, B., Windsor, J. A., Phillips, A. R. (2014) MicroRNAs in mesenteric lymph and plasma during acute pancreatitis. Ann. Surg. 260, 341-347. <https://doi.org/10.1097/SLA.0000000000000447>
7. Blondal, T., Jensby Nielsen, S., Baker, A., Andreasen, D., Mouritzen, P., Wrang Teilum, M., Dahlsveen, I. K. (2013) Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 59, S1-S6. <https://doi.org/10.1016/j.ymeth.2012.09.015>
8. van den Boorn, J. G., Dassler, J., Coch, C., Schlee, M., Hartmann, G. (2013) Exosomes as nucleic acid nanocarriers. Adv. Drug Deliv. Rev. 65, 331-335. <https://doi.org/10.1016/j.addr.2012.06.011>
9. Bryniarski, K., Ptak, W., Jayakumar, A., Püllmann, K., Caplan, M. J., Chairoungdua, A., Lu, J., Adams, B. D., Sikora, E., Nazimek, K., Marquez, S., Kleinstein, S. H., Sangwung, P., Iwakiri, Y., Delgato, E., Redegeld, F., Blokhuis, B. R., Wojcikowski, J., Daniel, A. W., Groot Kormelink, T., Askenase, P. W. (2013) Antigen-specific, antibody-coated, exosome-like nanovesicles deliver suppressor T-cell microRNA- 150 to effector T cells to inhibit contact sensitivity. J. Allergy Clin. Immunol. 132, 170-181. <https://doi.org/10.1016/j.jaci.2013.04.048>
10. Callari, M., Dugo, M., Musella, V., Marchesi, E., Chiorino, G., Grand, M. M., Pierotti, M. A., Daidone, M. G., Canevari, S., De Cecco, L. (2012) Comparison of microarray platforms for measuring differential microRNA expression in paired normal/cancer colon tissues. PLoS One 7, e45105. <https://doi.org/10.1371/journal.pone.0045105>
11. Chen, X., Ba, Y., Ma, L., Cai, X., Yin, Y., Wang, K., Guo, J., Zhang, Y., Chen, J., Guo, X., Li, Q., Li, X., Wang, W., Zhang, Y., Wang, J., Jiang, X., Xiang, Y., Xu, C., Zheng, P., Zhang, J., Li, R., Zhang, H., Shang, X., Gong, T., Ning, G., Wang, J., Zen, K., Zhang, J., Zhang, C. Y. (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 18, 997-1006. <https://doi.org/10.1038/cr.2008.282>
12. Chen, X., Liang, H., Guan, D., Wang, C., Hu, X., Cui, L., Chen, S., Zhang, C., Zhang, J., Zen, K., Zhang, C. Y. (2013) A combination of Let-7d, Let-7g and Let-7i serves as a stable reference for normalization of serum microRNAs. PLoS One 8, e79652. <https://doi.org/10.1371/journal.pone.0079652>
13. Cheng, H. H., Yi, H. S., Kim, Y., Kroh, E. M., Chien, J. W., Eaton, K. D., Goodman, M. T., Tait, J. F., Tewari, M., Pritchard, C. C. (2013) Plasma processing conditions substantially influence circulating microRNA biomarker levels. PLoS One 8, e64795. <https://doi.org/10.1371/journal.pone.0064795>
14. Chim, S. S., Shing, T. K., Hung, E. C., Leung, T. Y., Lau, T. K., Chiu, R. W., Lo, Y. M. (2008) Detection and characterization of placental microRNAs in maternal plasma. Clin. Chem. 54, 482-490. <https://doi.org/10.1373/clinchem.2007.097972>
15. Cocucci, E., Racchetti, G., Meldolesi, J. (2009) Shedding microvesicles: artefacts no more. Trends Cell. Biol. 19, 43-51. <https://doi.org/10.1016/j.tcb.2008.11.003>
16. Cortez, M. A., Calin, G. A. (2009) MicroRNA identification in plasma and serum: a new tool to diagnose and monitor diseases. Exp. Opin. Biol. Ther. 9, 703-711. <https://doi.org/10.1517/14712590902932889>
17. Creighton, C. J., Reid, J. G., Gunaratne, P. H. (2009) Expression profiling of microRNAs by deep sequencing. Brief Bioinform. 10, 490-497. <https://doi.org/10.1093/bib/bbp019>
18. Cuk, K., Zucknick, M., Heil, J., Madhavan, D., Schott, S., Turchinovich, A., Arlt, D., Rath, M., Sohn, C., Benner, A., Junkermann, H., Schneeweiss, A., Burwinkel, B. (2013) Circulating microRNAs in plasma as early detection markers for breast cancer. Int. J. Cancer 132, 1602-1612. <https://doi.org/10.1002/ijc.27799>
19. Diehl, P., Fricke, A., Sander, L., Stamm, J., Bassler, N., Htun, N., Ziemann, M., Helbing, T., El-Osta, A., Jowett, J. B., Peter, K. (2012) Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc. Res. 93, 633-644. <https://doi.org/10.1093/cvr/cvs007>
20. Duttagupta, R., Jiang, R., Gollub, J., Getts, R. C., Jones, K. W. (2011) Impact of cellular miRNAs on circulating miRNA biomarker signatures. PLoS One 6, e20769. <https://doi.org/10.1371/journal.pone.0020769>
21. El-Hefnawy, T., Raja, S., Kelly, L., Bigbee, W. L., Kirkwood, J. M., Luketich, J. D., Godfrey, T. E. (2004) Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics. Clin. Chem. 50, 564-573. <https://doi.org/10.1373/clinchem.2003.028506>
22. Fang, C., Zhu, D. X., Dong, H. J., Zhou, Z. J., Wang, Y. H., Liu, L., Fan, L., Miao, K. R., Liu, P., Xu, W., Li, J. Y. (2012) Serum microRNAs are promising novel biomarkers for diffuse large B cell lymphoma. Ann. Hematol. 91, 553-559. <https://doi.org/10.1007/s00277-011-1350-9>
23. Fayyad-Kazan, H., Bitar, N., Najar, M., Lewalle, P., Fayyad- Kazan, M., Badran, R., Hamade, E., Daher, A., Hussein, N., ElDirani, R., Berri, F., Vanhamme, L., Burny, A., Martiat, P., Rouas, R., Badran, B. (2013) Circulating miR- 150 and miR-342 in plasma are novel potential biomarkers for acute myeloid leukemia. J. Transl. Med. 11, 31. <https://doi.org/10.1186/1479-5876-11-31>
24. Fichtlscherer, S., Zeiher, A. M., Dimmeler, S. (2011) Circulating microRNAs: biomarkers or mediators of cardiovascular diseases? Arterioscler. Thromb. Vasc. Biol. 31, 2383-2390. <https://doi.org/10.1161/ATVBAHA.111.226696>
25. Filkova, M., Aradi, B., Senolt, L., Ospelt, C., Vettori, S., Mann, H., Filer, A., Raza, K., Buckley, C. D., Snow, M., Vencovsky, J., Pavelka, K., Michel, B. A., Gay, R. E., Gay, S., Jüngel, A. (2014) Association of circulating miR-223 and miR-16 with disease activity in patients with early rheumatoid arthritis. Ann. Rheum. Dis. 73, 1898-1904. <https://doi.org/10.1136/annrheumdis-2012-202815>
26. Fonsato, V., Collino, F., Herrera, M. B., Cavallari, C., Deregibus, M. C., Cisterna, B., Bruno, S., Romagnoli, R., Salizzoni, M., Tetta, C., Camussi, G. (2012) Human liver stem cell-derived microvesicles inhibit hepatoma growth in SCID mice by delivering antitumor microRNAs. Stem Cells 30, 1985-1998. <https://doi.org/10.1002/stem.1161>
27. Friedländer, M. R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., Knespel, S., Rajewsky, N. (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nat. Biotechnol. 26, 407-415. <https://doi.org/10.1038/nbt1394>
28. Gaughwin, P. M., Ciesla, M., Lahiri, N., Tabrizi, S. J., Brundin, P., Björkqvist, M. (2011) Hsa-miR-34b is a plasma-stable microRNA that is elevated in pre-manifest Huntington’s disease. Hum. Mol. Genet. 20, 2225-2237. <https://doi.org/10.1093/hmg/ddr111>
29. Ge, Q., Zhou, Y., Lu, J., Bai, Y., Xie, X., Lu, Z. (2014) miRNA in plasma exosome is stable under different storage conditions. Molecules 19, 1568-1575. <https://doi.org/10.3390/molecules19021568>
30. Ge, Q., Zhu, Y., Li, H., Tian, F., Xie, X., Bai, Y. (2015) Differential expression of circulating miRNAs in maternal plasma in pregnancies with fetal macrosomia. Int. J. Mol. Med. 35, 81-91. <https://doi.org/10.3892/ijmm.2014.1989>
31. Gilad, S., Meiri, E., Yogev, Y., Benjamin, S., Lebanony, D., Yerushalmi, N., Benjamin, H., Kushnir, M., Cholakh, H., Melamed, N., Bentwich, Z., Hod, M., Goren, Y., Chajut, A. (2008) Serum microRNAs are promising novel biomarkers. PLoS One. 3, e3148. <https://doi.org/10.1371/journal.pone.0003148>
32. Git, A., Dvinge, H., Salmon-Divon, M., Osborne, M., Kutter, C., Hadfield, J., Bertone, P., Caldas, C. (2010) Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression. RNA 16, 991-1006. <https://doi.org/10.1261/rna.1947110>
33. Godfrey, A. C., Xu, Z., Weinberg, C. R., Getts, R. C., Wade, P. A., DeRoo, L. A., Sandler, D. P., Taylor, J. A. (2013) Serum microRNA expression as an early marker for breast cancer risk in prospectively collected samples from the Sister Study cohort. Breast Cancer Res. 15, R42. <https://doi.org/10.1186/bcr3428>
34. Gomes, C. P. C., Cho, J.-H., Hood, L., Franco, O. L., Pereira, R. W., Wang, K. (2013) A review of computational tools in microRNA discovery. Front. Genet. 4, 81. <https://doi.org/10.3389/fgene.2013.00081>
35. Grasedieck, S., Sorrentino, A., Langer, C., Buske, C., Döhner, H., Mertens, D., Kuchenbauer, F. (2013) Circulating microRNAs in hematological diseases: principles, challenges, and perspectives. Blood 121, 4977-4984. <https://doi.org/10.1182/blood-2013-01-480079>
36. Gu, H., Li, H., Zhang, L., Luan, H., Huang, T., Wang, L., Fan, Y., Zhang, Y., Liu, X., Wang, W., Yuan, Z. (2012) Diagnostic role of microRNA expression profile in the serum of pregnant women with fetuses with neural tube defects. J. Neurochem. 122, 641-649. <https://doi.org/10.1111/j.1471-4159.2012.07812.x>
37. Gunel, T., Zeybek, Y. G., Akçakaya, P., Kalelioğlu, I., Benian, A., Ermis, H., Aydınlı, K. (2011) Serum microRNA expression in pregnancies with preeclampsia. Genet. Mol. Res. 10, 4034-4040. <https://doi.org/10.4238/2011.November.8.5>
38. Hackenberg, M., Sturm, M., Langenberger, D., Falcón-Pérez, J. M., Aransay, A. M. (2009) miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments. Nucleic Acids Res. 37, 68-76. <https://doi.org/10.1093/nar/gkp347>
39. Han, H. S., Jo, Y. N., Lee, J. Y., Choi, S. Y., Jeong, Y., Yun, J., Lee, O. J. (2014) Identification of suitable reference genes for the relative quantification of microRNAs in pleural effusion. Oncol. Lett. 8, 1889-1895. <https://doi.org/10.3892/ol.2014.2404>
40. Hanke, M., Hoefig, K., Merz, H., Feller, A. C., Kausch, I., Jocham, D., Warnecke, J. M., Sczakiel, G. (2010) A robust methodology to study urine microRNA as tumor marker: microRNA-126 and microRNA-182 are related to urinary bladder cancer. Urol. Oncol. 28, 655-661. <https://doi.org/10.1016/j.urolonc.2009.01.027>
41. He, L., Hannon, G. J. (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522-531. <https://doi.org/10.1038/nrg1379>
42. Hindson, C. M., Chevillet, J. R., Briggs, H. A., Gallichotte, E. N., Ruf, I. K., Hindson, B. J., Vessella, R. L., Tewari, M. (2013) Absolute quantification by droplet digital PCR versus analog real-time PCR. Nat. Methods 10, 1003-1005. <https://doi.org/10.1038/nmeth.2633>
43. Ho, A. S., Huang, X., Cao, H., Christman-Skieller, C., Bennewith, K., Le, Q. T., Koong, A. C. (2010) Circulating miR-210 as a novel hypoxia marker in pancreatic cancer. Transl. Oncol. 3, 109-113. <https://doi.org/10.1593/tlo.09256>
44. de Hoon, M., Hayashizaki, Y. (2008) Deep cap analysis gene expression (CAGE): genome-wide identification of promoters, quantification of their expression, and network inference. Biotechniques 44, 627-632. <https://doi.org/10.2144/000112802>
45. Huang, J. J., Yu, J., Li, J. Y., Liu, Y. T., Zhong, R. Q. (2012) Circulating microRNA expression is associated with genetic subtype and survival of multiple myeloma. Med. Oncol. 29, 2402-2408. <https://doi.org/10.1007/s12032-012-0210-3>
46. Hunter, M. P., Ismail, N., Zhang, X., Aguda, B. D., Lee, E. J., Yu, L., Xiao, T., Schafer, J., Lee, M. L., Schmittgen, T. D., Nana-Sinkam, S. P., Jarjoura, D., Marsh, C. B. (2008) Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3, e3694. <https://doi.org/10.1371/journal.pone.0003694>
47. Ilhan-Mutlu, A., Wagner, L., Wöhrer, A., Furtner, J., Widhalm, G., Marosi, C., Preusser, M. (2012) Plasma microRNA-21 concentration may be a useful biomarker in glioblastoma patients. Cancer Invest. 30, 615-621. <https://doi.org/10.3109/07357907.2012.708071>
48. Ishihara, K., Sasaki, D., Tsuruda, K., Inokuchi, N., Nagai, K., Hasegawa, H., Yanagihara, K., Kamihira, S. (2012) Impact of miR-155 and miR-126 as novel biomarkers on the assessment of disease progression and prognosis in adult T-cell leukemia. Cancer Epidemiol. 36, 560-565. <https://doi.org/10.1016/j.canep.2012.07.002>
49. Jin, X. F., Wu, N., Wang, L., Li, J. (2013) Circulating microRNAs: a novel class of potential biomarkers for diagnosing and prognosing central nervous system diseases. Cell. Mol. Neurobiol. 33, 601-613. <https://doi.org/10.1007/s10571-013-9940-9>
50. Jones, C. I., Zabolotskaya, M. V., King, A. J., Stewart, H. J., Horne, G. A., Chevassut, T. J., Newbury, S. F. (2012) Identification of circulating microRNAs as diagnostic biomarkers for use in multiple myeloma. Br. J. Cancer 107, 1987-1996. <https://doi.org/10.1038/bjc.2012.525>
51. Jones, K., Nourse, J. P., Keane, C., Bhatnagar, A., Gandhi, M. K. (2014) Plasma microRNA are disease response biomarkers in classical Hodgkin lymphoma. Clin. Cancer Res. 20, 253-264. <https://doi.org/10.1158/1078-0432.CCR-13-1024>
52. Jung, E. J., Santarpia, L., Kim, J., Esteva, F. J., Moretti, E., Buzdar, A. U., Di Leo, A., Le, X. F., Bast, R. C. Jr, Park, S. T., Pusztai, L., Calin, G. A. (2012) Plasma microRNA 210 levels correlate with sensitivity to trastuzumab and tumor presence in breast cancer patients. Cancer 118, 2603-2614. <https://doi.org/10.1002/cncr.26565>
53. Kirschner, M. B., Kao, S. C., Edelman, J. J., Armstrong, N. J., Vallely, M. P., van Zandwijk, N., Reid, G. (2011) Haemolysis during sample preparation alters microRNA content of plasma. PLoS One 6, e24145. <https://doi.org/10.1371/journal.pone.0024145>
54. Kroh, E. M., Parkin, R. K., Mitchell, P. S., Tewari, M. (2010) Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 50, 298-301. <https://doi.org/10.1016/j.ymeth.2010.01.032>
55. Laterza, O. F., Lim, L., Garrett-Engele, P. W., Vlasakova, K., Muniappa, N., Tanaka, W. K., Johnson, J. M., Sina, J. F., Fare, T. L., Sistare, F. D., Glaab, W. E. (2009) Plasma microRNAs as sensitive and specific biomarkers of tissue injury. Clin. Chem. 55, 1977-1983. <https://doi.org/10.1373/clinchem.2009.131797>
56. Lawrie, C. H., Gal, S., Dunlop, H. M., Pushkaran, B., Liggins, A. P., Pulford, K., Banham, A. H., Pezzella, F., Boultwood, J., Wainscoat, J. S., Hatton, C. S., Harris, A. L. (2008) Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br. J. Haematol. 141, 672-675. <https://doi.org/10.1111/j.1365-2141.2008.07077.x>
57. Lewis A. P., Jopling C. L. (2010) Regulation and biological function of the liver-specific miR-122. Biochem. Soc. Trans. 38, 1553-1557. <https://doi.org/10.1042/BST0381553>
58. Lewis, B. P., Burge, C. B., Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20. <https://doi.org/10.1016/j.cell.2004.12.035>
59. Li, H., Guo, L., Wu, Q., Lu, J., Ge, Q., Lu, Z. (2012) A comprehensive survey of maternal plasma miRNAs expression profiles using high-throughput sequencing. Clin. Chim. Acta 413, 568-576. <https://doi.org/10.1016/j.cca.2011.11.026>
60. Li, H., Ge, Q., Guo, L., Lu, Z. (2013) Maternal plasma miRNAs expression in preeclamptic pregnancies. Biomed. Res. Int. 2013, 970265.
61. Li, Y., Kowdley, K. V. (2012) Method for microRNA isolation from clinical serum samples. Anal. Biochem. 431, 69-75. <https://doi.org/10.1016/j.ab.2012.09.007>
62. Liang, Y., Ridzon, D., Wong, L., Chen, C. (2007) Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 8, 166. <https://doi.org/10.1186/1471-2164-8-166>
63. Liu, X. G., Zhu, W. Y., Huang, Y. Y., Ma, L .N., Zhou, S. Q., Wang, Y. K., Zeng, F., Zhou, J. H., Zhang, Y. K. (2012) High expression of serum miR-21 and tumor miR-200c associated with poor prognosis in patients with lung cancer. Med. Oncol. 29, 618-626. <https://doi.org/10.1007/s12032-011-9923-y>
64. Liu, X., Zhang, L., Cheng, K., Wang, X., Ren, G., Xie, P. (2014) Identification of suitable plasma-based reference genes for miRNAome analysis of major depressive disorder. J. Affect. Disord. 163, 133-139. <https://doi.org/10.1016/j.jad.2013.12.035>
65. Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A., Downing, J. R., Jacks, T., Horvitz, H. R., Golub, T. R. (2005) MicroRNA expression profiles classify human cancers. Nature 435, 834-838. <https://doi.org/10.1038/nature03702>
66. Luo, W., Nie, Q., Zhang, X. (2013) MicroRNAs involved in skeletal muscle differentiation. J. Genet. Genomics 40, 107-116. <https://doi.org/10.1016/j.jgg.2013.02.002>
67. Matsumura, H., Yoshida, K., Luo, S., Kimura, E., Fujibe, T., Albertyn, Z., Barrero, R. A., Krüger, D. H., Kahl, G., Schroth, G. P., Terauchi, R. (2010) High-throughput SuperSAGE for digital gene expression analysis of multiple samples using next generation sequencing. PLoS One 5, e12010. <https://doi.org/10.1371/journal.pone.0012010>
68. Miotto, E., Saccenti, E., Lupini, L., Callegari, E., Negrini, M., Ferracin, M. (2014) Quantification of circulating miRNAs by droplet digital PCR: comparison of EvaGreen- and TaqMan-based chemistries. Cancer Epidemiol. Biomarkers Prev. 23, 2638-2642. <https://doi.org/10.1158/1055-9965.EPI-14-0503>
69. Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L., Peterson, A., Noteboom, J., O’Briant, K. C., Allen, A., Lin, D. W., Urban, N., Drescher, C. W., Knudsen, B. S., Stirewalt, D. L., Gentleman, R., Vessella, R. L., Nelson, P. S., Martin, D. B., Tewari, M. (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. USA 105, 10513-10518. <https://doi.org/10.1073/pnas.0804549105>
70. Miura, K., Miura, S., Yamasaki, K., Higashijima, A., Kinoshita, A., Yoshiura, K., Masuzaki, H. (2010) Identification of pregnancy-associated microRNAs in maternal plasma. Clin. Chem. 56, 1767-1771. <https://doi.org/10.1373/clinchem.2010.147660>
71. Monleau, M., Bonnel, S., Gostan, T., Blanchard, D., Courgnaud, V., Lecellier. C. H. (2014) Comparison of different extraction techniques to profile microRNAs from human sera and peripheral blood mononuclear cells. BMC Genomics 15, 395. <https://doi.org/10.1186/1471-2164-15-395>
72. Moret, I., Sánchez-Izquierdo, D., Iborra, M., Tortosa, L., Navarro-Puche, A., Nos, P., Cervera, J., Beltrán, B. (2013) Assessing an improved protocol for plasma microRNA extraction. PLoS One 8, e82753. <https://doi.org/10.1371/journal.pone.0082753>
73. Mouillet, J. F., Chu, T., Hubel, C. A., Nelson, D. M., Parks, W. T., Sadovsky, Y. (2010) The levels of hypoxia-regulated microRNAs in plasma of pregnant women with fetal growth restriction. Placenta 31, 781-784. <https://doi.org/10.1016/j.placenta.2010.07.001>
74. Moussay, E., Wang, K., Cho, J. H., van Moer, K., Pierson, S., Paggetti, J., Nazarov, P. V., Palissot, V., Hood, L. E., Berchem, G., Galas, D. J. (2011) MicroRNA as biomarkers and regulators in B-cell chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA 108, 6573-6578. <https://doi.org/10.1073/pnas.1019557108>
75. Muralidharan-Chari, V., Clancy, J. W., Sedgwick, A., D’Souza-Schorey, C. (2010) Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 123, 1603-1611. <https://doi.org/10.1242/jcs.064386>
76. Ng, E. K., Chong, W. W., Jin, H., Lam, E. K., Shin, V. Y., Yu, J., Poon, T. C., Ng, S. S., Sung, J. J. (2009) Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut 58, 1375-1381. <https://doi.org/10.1136/gut.2008.167817>
77. Nielsen, L. B., Wang, C., Sørensen, K., Bang-Berthelsen, C. H., Hansen, L., Andersen, M. L., Hougaard, P., Juul, A., Zhang, C. Y., Pociot, F., Mortensen, H. B. (2012) Circulating levels of microRNA from children with newly diagnosed type 1 diabetes and healthy controls: evidence that miR-25 associates to residual β-cell function and glycaemic control during disease progression. Exp. Diabetes Res. 2012, 896362.
78. Noren Hooten, N., Fitzpatrick, M., Wood, W. H., De, S., Ejiogu, N., Zhang, Y., Mattison, J. A., Becker, K. G., Zonderman, A. B., Evans, M. K. (2013) Age-related changes in microRNA levels in serum. Aging 5, 725-740.
79. O’Driscoll, L. (2007) Extracellular nucleic acids and their potential as diagnostic, prognostic and predictive biomarkers. Anticancer Res. 27, 1257-1265.
80. Ohyashiki, J. H., Umezu, T., Kobayashi, C., Hamamura, R. S., Tanaka, M., Kuroda, M., Ohyashiki, K. (2010) Impact on cell to plasma ratio of miR-92a in patients with acute leukemia: in vivo assessment of cell to plasma ratio of miR- 92a. BMC Res. Notes 3, 347. <https://doi.org/10.1186/1756-0500-3-347>
81. Ohyashiki, K., Umezu, T., Yoshizawa, S., Ito, Y., Ohyashiki, M., Kawashima, H., Tanaka, M., Kuroda, M., Ohyashiki, J. H. (2011) Clinical impact of down-regulated plasma miR-92a levels in non-Hodgkin’s lymphoma. PLoS One 6, e16408. <https://doi.org/10.1371/journal.pone.0016408>
82. Ortega, F. J., Mercader, J. M., Catalán, V., Moreno-Navarrete, J. M., Pueyo, N., Sabater, M., Gómez-Ambrosi, J., Anglada, R., Fernández-Formoso, J. A., Ricart, W., Frühbeck, G., Fernández-Real, J. M. (2013) Targeting the circulating microRNA signature of obesity. Clin. Chem. 59, 781-792. <https://doi.org/10.1373/clinchem.2012.195776>
83. Oulas, A., Boutla, A., Gkirtzou, K., Reczko, M., Kalantidis, K., Poirazi, P. (2009) Prediction of novel microRNA genes in cancer-associated genomic regions – a combined computational and experimental approach. Nucleic Acids Res. 37, 3276-3287. <https://doi.org/10.1093/nar/gkp120>
84. Park, N. J., Zhou, H., Elashoff, D., Henson, B. S., Kastratovic, D. A., Abemayor, E., Wong, D. T. (2009) Salivary micro- RNA: discovery, characterization, and clinical utility for oral cancer detection. Clin. Cancer Res. 15, 5473-5477. <https://doi.org/10.1158/1078-0432.CCR-09-0736>
85. Pradervand, S., Weber, J., Lemoine, F., Consales, F., Paillusson, A., Dupasquier, M., Thomas, J., Richter, H., Kaessmann, H., Beaudoing, E., Hagenbüchle, O., Harshman, K. (2010) Concordance among digital gene expression, microarrays, and qPCR when measuring differential expression of microRNAs. Biotechniques 48, 219-222. <https://doi.org/10.2144/000113367>
86. Prats-Puig, A., Ortega, F. J., Mercade, J. M., Moreno-Navarrete, J. M., Moreno, M., Bonet, N., Ricart, W., López- Bermejo, A., Fernández-Real, J. M. (2013) Changes in circulating microRNAs are associated with childhood obesity. J. Clin. Endocrinol. Metab. 98, 1655-1660. <https://doi.org/10.1210/jc.2013-1496>
87. Pritchard, C. C., Kroh, E., Wood, B., Arroyo, J. D., Dougherty, K. J., Miyaji, M. M., Tait, J. F., Tewari, M. (2012) Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev. Res. 5, 492-497. <https://doi.org/10.1158/1940-6207.CAPR-11-0370>
88. Rabinowits, G., Gerçel-Taylor, C., Day, J. M., Taylor, D. D., Kloecker, G. H. (2009) Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer 10, 42-46. <https://doi.org/10.3816/CLC.2009.n.006>
89. Rasmussen, K. D., Simmini, S., Abreu-Goodger, C., Bartonicek, N., Di Giacomo, M., Bilbao-Cortes, D., Horos, R., Von Lindern, M., Enright, A. J., O’Carroll, D. (2010) The miR-144/451 locus is required for erythroid homeostasis. J. Exp. Med. 207, 1351-1358. <https://doi.org/10.1084/jem.20100458>
90. Rekker, K., Saare, M., Roost, A. M., Salumets, A., Peters, M. (2013) Circulating microRNA profile throughout the menstrual cycle. PLoS One 8, e81166. <https://doi.org/10.1371/journal.pone.0081166>
91. Resnick, K. E., Alder, H., Hagan, J. P., Richardson, D. L., Croce, C. M., Cohn, D. E. (2009) The detection of differentially expressed microRNAs from the serum of ovarian cancer patients using a novel real-time PCR platform. Gynecol. Oncol. 112, 55-59. <https://doi.org/10.1016/j.ygyno.2008.08.036>
92. van Rooij, E., Sutherland, L. B., Qi, X., Richardson, J. A., Hill, J., Olson, E. N. (2007) Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575-579. <https://doi.org/10.1126/science.1139089>
93. Russo, F., Di Bella, S., Nigita, G., Macca, V., Laganà, A., Giugno, R., Pulvirenti, A., Ferro, A. (2012) miRandola: extracellular circulating microRNAs database. PLoS One 7, e47786. <https://doi.org/10.1371/journal.pone.0047786>
94. Schmittgen, T. D., Lee, E. J., Jiang, J. (2008) High-throughput real-time PCR. Methods Mol. Biol. 429, 89-98. <https://doi.org/10.1007/978-1-60327-040-3_7>
95. Shen, J., Liu, Z., Todd, N. W., Zhang, H., Liao, J., Yu, L., Guarnera, M. A., Li, R., Cai, L., Zhan, M., Jiang, F. (2011) Diagnosis of lung cancer in individuals with solitary pulmonary nodules by plasma microRNA biomarkers. BMC Cancer 11, 374. <https://doi.org/10.1186/1471-2407-11-374>
96. Simpson, R. J., Lim, J. W., Moritz, R. L., Mathivanan, S. (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev. Proteomics 6, 267-283. <https://doi.org/10.1586/epr.09.17>
97. Steudemann, C., Bauersachs, S., Weber, K., Wess, G. (2013) Detection and comparison of microRNA expression in the serum of Doberman Pinschers with dilated cardiomyopathy and healthy controls. BMC Vet. Res. 9, 12. <https://doi.org/10.1186/1746-6148-9-12>
98. Sun, A. X., Crabtree, G. R., Yoo, A. S. (2013a) MicroRNAs: regulators of neuronal fate. Curr. Opin. Cell Biol. 25, 215-221. <https://doi.org/10.1016/j.ceb.2012.12.007>
99. Sun, L., Hu, J., Xiong, W., Chen, X., Li, H., Jie, S. (2013b) MicroRNA expression profiles of circulating microvesicles in hepatocellular carcinoma. Acta Gastroenterol. Belg. 76, 386-392.
100. Sun, Y., Wang, M., Lin, G., Sun, S., Li, X., Qi, J., Li, J. (2012) Serum microRNA-155 as a potential biomarker to track disease in breast cancer. PLoS One 7, e47003. <https://doi.org/10.1371/journal.pone.0047003>
101. Tan, L., Yu, J. T., Liu, Q. Y., Tan, M. S., Zhang, W., Hu, N., Wang, Y. L., Sun, L., Jiang, T., Tan, L. (2014) Circulating miR-125b as a biomarker of Alzheimer’s disease. J. Neurol. Sci. 336, 52-56. <https://doi.org/10.1016/j.jns.2013.10.002>
102. Tanaka, M., Oikawa, K., Takanashi, M., Kudo, M., Ohyashiki, J., Ohyashiki, K., Kuroda, M. (2009) Down-regulation of miR-92 in human plasma is a novel marker for acute leukemia patients. PLoS One 4, e5532. <https://doi.org/10.1371/journal.pone.0005532>
103. Tang, D., Shen, Y., Wang, M., Yang, R., Wang, Z., Sui, A., Jiao, W., Wang, Y. (2013) Identification of plasma microRNAs as novel noninvasive biomarkers for early detection of lung cancer. Eur. J. Cancer Prev. 22, 540-548. <https://doi.org/10.1097/CEJ.0b013e32835f3be9>
104. Tsui, N. B., Ng, E. K., Lo, Y. M. (2002) Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clin. Chem. 48, 1647-1653. <https://doi.org/10.1093/clinchem/48.10.1647>
105. Turchinovich, A., Weiz, L., Langheinz, A., Burwinkel, B. (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res. 39, 7223-7233. <https://doi.org/10.1093/nar/gkr254>
106. Umezu, T., Ohyashiki, K., Kuroda, M., Ohyashiki, J. H. (2013) Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene 32, 2747-2755. <https://doi.org/10.1038/onc.2012.295>
107. Ura, B., Feriotto, G., Monasta, L., Bilel, S., Zweyer, M., Celeghini, C. (2014) Potential role of circulating microRNAs as early markers of preeclampsia. Taiwan J. Obstet. Gynecol. 53, 232-234. <https://doi.org/10.1016/j.tjog.2014.03.001>
108. Vickers, K. C., Palmisano, B. T., Shoucri, B. M., Shamburek, R. D., Remaley, A. T. (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 13, 423-433. <https://doi.org/10.1038/ncb2210>
109. Villar, A. V., García, R., Merino, D., Llano, M., Cobo, M., Montalvo, C., Martín-Durán, R., Hurlé, M. A., Nistal, J. F. (2013) Myocardial and circulating levels of microRNA-21 reflect left ventricular fibrosis in aortic stenosis patients. Int. J. Cardiol. 167, 2875-2881. <https://doi.org/10.1016/j.ijcard.2012.07.021>
110. Villarroya-Beltri, C., Gutiérrez-Vázquez, C., Sánchez-Cabo, F., Pérez-Hernández, D., Vázquez, J., Martin-Cofreces, N., Martinez-Herrera, D. J., Pascual-Montano, A., Mittelbrunn, M., Sánchez-Madrid, F. (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun. 4, 2980. <https://doi.org/10.1038/ncomms3980>
111. Wang, B., Howel, P., Bruheim, S., Ju, J., Owen, L. B., Fodstad, O., Xi, Y. (2011) Systematic evaluation of three microRNA profiling platforms: microarray, beads array, and quantitative real-time PCR array. PLoS One 6, e17167. <https://doi.org/10.1371/journal.pone.0017167>
112. Wang, B., Zhang, Q. (2012) The expression and clinical significance of circulating microRNA-21 in serum of five solid tumors. J. Cancer Res. Clin. Oncol. 138, 1659-1666. <https://doi.org/10.1007/s00432-012-1244-9>
113. Wang, G. K., Zhu, J. Q., Zhang, J. T., Li, Q., Li, Y., He, J., Qin, Y. W., Jing, Q. (2010b) Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur. Heart J. 31, 659-666. <https://doi.org/10.1093/eurheartj/ehq013>
114. Wang, H. J., Zhang, P. J., Chen, W. J., Jie, D., Dan, F., Jia, Y. H., Xie, L. X. (2013) Characterization and identification of novel serum microRNAs in sepsis patients with different outcomes. Shock 39, 480-487. <https://doi.org/10.1097/SHK.0b013e3182940cb8>
115. Wang, K., Zhang, S., Weber, J., Baxter, D., Galas, D. J. (2010a) Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 38, 7248-7259. <https://doi.org/10.1093/nar/gkq601>
116. Wang, K., Yuan, Y., Cho, J. H., McClarty, S., Baxter, D., Galas, D. J. (2012a) Comparing the microRNA spectrum between serum and plasma. PLoS One 7, e41561. <https://doi.org/10.1371/journal.pone.0041561>
117. Wang, Q., Huang, Z., Ni, S., Xiao, X., Xu, Q., Wang, L., Huang, D., Tan, C., Sheng, W., Du, X. (2012b) Plasma miR-601 and miR-760 are novel biomarkers for the early detection of colorectal cancer. PLoS One 7, e44398. <https://doi.org/10.1371/journal.pone.0044398>
118. Wang, Z., Gerstein, M., Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63. <https://doi.org/10.1038/nrg2484>
119. Weber, J. A., Baxter, D. H., Zhang, S., Huang, D. Y., Huang, K. H., Lee, M. J., Galas, D. J., Wang, K. (2010) The micro-RNA spectrum in 12 body fluids. Clin. Chem. 56, 1733-1741. <https://doi.org/10.1373/clinchem.2010.147405>
120. Wei, H., Yuan, Y., Liu, S., Wang, C., Yang, F., Lu, Z., Wang, C., Deng, H., Zhao, J., Shen, Y., Zhang, C., Yu, X., Xu, Q. (2015) Detection of circulating miRNA levels in schizophrenia. Am. J. Psychiatry appiajp201514030273.
121. Wei, J., Gao, W., Zhu, C. J., Liu, Y. Q., Mei, Z., Cheng, T., Shu, Y. Q. (2011) Identification of plasma microRNA-21 as a biomarker for early detection and chemosensitivity of non-small cell lung cancer. Chin. J. Cancer 30, 407-414. <https://doi.org/10.5732/cjc.010.10522>
122. Williams, Z., Ben-Dov, I. Z., Elias, R., Mihailovic, A., Brown, M., Rosenwaks, Z., Tuschl, T. (2013) Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Proc. Natl. Acad. Sci. USA 110, 4255-4260. <https://doi.org/10.1073/pnas.1214046110>
123. Xiang, M., Zeng, Y., Yang, R., Xu, H., Chen, Z., Zhong, J., Xie, H., Xu, Y., Zeng, X. (2014) U6 is not a suitable endogenous control for the quantification of circulating microRNAs. Biochem. Biophys. Res. Commun. 454, 210-214. <https://doi.org/10.1016/j.bbrc.2014.10.064>
124. Xu, J., Wu, C., Che, X., Wang, L., Yu, D., Zhang, T., Huang, L., Li, H., Tan, W., Wang, C., Lin, D. (2011) Circulating microRNAs, miR-21, miR-122, and miR-223, in patients with hepatocellular carcinoma or chronic hepatitis. Mol. Carcinog. 50, 136-142. <https://doi.org/10.1002/mc.20712>
125. Xu, P., Zhao, Y., Liu, M., Wang, Y., Wang, H., Li, Y. X., Zhu, X., Yao, Y., Wang, H., Qiao, J., Ji, L., Wang, Y. L. (2014) Variations of microRNAs in human placentas and plasma from preeclamptic pregnancy. Hypertension 63, 1276-1284. <https://doi.org/10.1161/HYPERTENSIONAHA.113.02647>
126. Yaman Agaoglu, F., Kovancilar, M., Dizdar, Y., Darendeliler, E., Holdenrieder, S., Dalay, N., Gezer, U. (2011) Investigation of miR-21, miR-141, and miR-221 in blood circulation of patients with prostate cancer. Tumour Biol. 32, 583-588. <https://doi.org/10.1007/s13277-011-0154-9>
127. Yokota, M., Tatsumi, N., Nathalang, O., Yamada, T., Tsuda, I. (1999) Effects of heparin on polymerase chain reaction for blood white cells. J. Clin. Lab. Anal. 13, 133-140. <https://doi.org/10.1002/(SICI)1098-2825(1999)13:3<133::AID-JCLA8>3.0.CO;2-0>
128. Yoshizawa, S., Ohyashiki, J. H., Ohyashiki, M., Umezu, T., Suzuki, K., Inagaki, A., Iida, S., Ohyashiki, K. (2012) Downregulated plasma miR-92a levels have clinical impact on multiple myeloma and related disorders. Blood Cancer J. 2, e53. <https://doi.org/10.1038/bcj.2011.51>
129. Yuan, A., Farber, E. L., Rapoport, A. L., Tejada, D., Deniskin, R., Akhmedov, N. B., Farber, D. B. (2009) Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4, e4722. <https://doi.org/10.1371/journal.pone.0004722>
130. Yuana, Y., Levels, J., Grootemaat, A., Sturk, A., Nieuwland, R. (2014) Co-isolation of extracellular vesicles and highdensity lipoproteins using density gradient ultracentrifugation. J. Extracell. Vesicles 3, 1-5. <https://doi.org/10.3402/jev.v3.23262>
131. Zahm, A. M., Thayu, M., Hand, N. J., Horner, A., Leonard, M. B., Friedman, J. R. (2011) Circulating microRNA is a biomarker of pediatric Crohn disease. J. Pediatr. Gastroenterol. Nutr. 53, 26-33. <https://doi.org/10.1097/MPG.0b013e31822200cc>
132. Zearo, S., Kim, E., Zhu, Y., Zhao, J. T., Sidhu, S. B., Robinson, B. G., Soon, P. S. (2014) MicroRNA-484 is more highly expressed in serum of early breast cancer patients compared to healthy volunteers. BMC Cancer 14, 200. <https://doi.org/10.1186/1471-2407-14-200>
133. Zeng, R. C., Zhang, W., Yan, X. Q., Ye, Z. Q., Chen, E. D., Huang, D. P., Zhang, X. H., Huang, G. L. (2013) Downregulation of miRNA-30a in human plasma is a novel marker for breast cancer. Med. Oncol. 30, 477. <https://doi.org/10.1007/s12032-013-0477-z>
134. Zernecke, A., Bidzhekov, K., Noels, H., Shagdarsuren, E., Gan, L., Denecke, B., Hristov, M., Köppel, T., Jahantigh, M. N., Lutgens, E., Wang, S., Olson, E. N., Schober, A., Weber, C. (2009) Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signal. 2, ra81. <https://doi.org/10.1126/scisignal.2000610>
135. Zhao, A., Li, G., Péoc’h, M., Genin, C., Gigante, M. (2013) Serum miR-210 as a novel biomarker for molecular diagnosis of clear cell renal cell carcinoma. Exp. Mol. Pathol. 94, 115-120. <https://doi.org/10.1016/j.yexmp.2012.10.005>
136. Zheng, G., Wang, H., Zhang, X., Yang, Y., Wang, L., Du, L., Li, W., Li, J., Qu, A., Liu, Y., Wang, C. (2013) Identification and validation of reference genes for qPCR detection of serum microRNAs in colorectal adenocarcinoma patients. PLoS One 8, e83025. <https://doi.org/10.1371/journal.pone.0083025>
137. Zhi, F., Cao, X., Xie, X., Wang, B., Dong, W., Gu, W., Ling, Y., Wang, R., Yang, Y., Liu, Y. (2013) Identification of circulating microRNAs as potential biomarkers for detecting acute myeloid leukemia. PLoS One 8, e56718. <https://doi.org/10.1371/journal.pone.0056718>
138. Zhu, S., Cao, L., Zhu, J., Kong, L., Jin, J., Qian, L., Zhu, C., Hu, X., Li, M., Guo, X., Han, S., Yu, Z. (2013) Identification of maternal serum microRNAs as novel non-invasive biomarkers for prenatal detection of fetal congenital heart defects. Clin. Chim. Acta 424, 66-72. <https://doi.org/10.1016/j.cca.2013.05.010>
139. Zhu, W., Qin, W., Atasoy, U., Sauter, E. R. (2009) Circulating microRNAs in breast cancer and healthy subjects. BMC Res. Notes 2, 89. <https://doi.org/10.1186/1756-0500-2-89>
140. Zomer, A., Vendrig, T., Hopmans, E. S., van Eijndhoven, M., Middeldorp, J. M., Pegtel, D. M. (2010) Exosomes: fit to deliver small RNA. Commun. Integr. Biol. 3, 447-450. <https://doi.org/10.4161/cib.3.5.12339>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive