Circulating microRNAs in cancer: Hope or hype?

Cancer Letters

Volumn 381, Issue 1, 2016, Pages 113-121

  Singh, Rajbir ^a   Ramasubramanian, Brinda ^a   Kanji, Suman ^a   Chakraborty, Arup R ^a   Haque, Saikh Jaharul ^a   Chakravarti, Arnab ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Biomarkers; Cancer; Circulating miRNA; Specificity; Translation

Indexed keywords

CIRCULATING MIRNA PROTEIN; MICRORNA; TUMOR MARKER; UNCLASSIFIED DRUG; RNA;

HOPE; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MICROARRAY ANALYSIS; MOLECULAR BIOLOGY; MOLECULAR PROBE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RNA ANALYSIS; RNA ISOLATION; RNA PURIFICATION; RNA TRANSPORT; SHORT SURVEY; ANIMAL; BLOOD; GENE THERAPY; GENETICS; MOLECULAR DIAGNOSIS; NEOPLASMS; PATHOLOGY; PREDICTIVE VALUE; PROCEDURES; PROGNOSIS;

ANIMALS; BIOMARKERS, TUMOR; GENETIC THERAPY; HUMANS; MICRORNAS; MOLECULAR DIAGNOSTIC TECHNIQUES; NEOPLASMS; PREDICTIVE VALUE OF TESTS; PROGNOSIS; RNA, NEOPLASM;

EID: 84979944343     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.07.002     Document Type: Review

References (114)

1. [1] Lee, R.C., Feinbaum, R.L., Ambros, V., The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75 (1993), 843–854.
2. [2] Schwarzenbach, H., Nishida, N., Calin, G.A., Pantel, K., Clinical relevance of circulating cell-free microRNAs in cancer. Nat. Rev. Clin. Oncol 11 (2014), 145–156.
3. [3] Kawaguchi, T., Komatsu, S., Ichikawa, D., Morimura, R., Tsujiura, M., Konishi, H., et al. Clinical impact of circulating miR-221 in plasma of patients with pancreatic cancer. Br. J. Cancer 108 (2013), 361–369.
4. [4] Ouyang, H., Gore, J., Deitz, S., Korc, M., microRNA-10b enhances pancreatic cancer cell invasion by suppressing TIP30 expression and promoting EGF and TGF-beta actions. Oncogene 33 (2014), 4664–4674.
5. [5] Zanutto, S., Pizzamiglio, S., Ghilotti, M., Bertan, C., Ravagnani, F., Perrone, F., et al. Circulating miR-378 in plasma: a reliable, haemolysis-independent biomarker for colorectal cancer. Br. J. Cancer 110 (2014), 1001–1007.
6. [6] Zhu, H., Fan, G.C., Extracellular/circulating microRNAs and their potential role in cardiovascular disease. Am. J. Cardiovasc. Dis 1 (2011), 138–149.
7. [7] Khvorova, A., Reynolds, A., Jayasena, S.D., Functional siRNAs and miRNAs exhibit strand bias. Cell 115 (2003), 209–216.
8. [8] Park, J.E., Heo, I., Tian, Y., Simanshu, D.K., Chang, H., Jee, D., et al. Dicer recognizes the 5′ end of RNA for efficient and accurate processing. Nature 475 (2011), 201–205.
9. [9] Morozova, N., Zinovyev, A., Nonne, N., Pritchard, L.L., Gorban, A.N., Harel-Bellan, A., Kinetic signatures of microRNA modes of action. RNA 18 (2012), 1635–1655.
10. [10] Cheng, G., Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Adv. Drug Deliv. Rev 81 (2015), 75–93.
11. [11] Jarry, J., Schadendorf, D., Greenwood, C., Spatz, A., van Kempen, L.C., The validity of circulating microRNAs in oncology: five years of challenges and contradictions. Mol. Oncol 8 (2014), 819–829.
12. [12] Koberle, V., Pleli, T., Schmithals, C., Augusto Alonso, E., Haupenthal, J., Bonig, H., et al. Differential stability of cell-free circulating microRNAs: implications for their utilization as biomarkers. PLoS ONE, 8, 2013 e75184.
13. [13] Witwer, K.W., Circulating microRNA biomarker studies: pitfalls and potential solutions. Clin. Chem 61 (2015), 56–63.
14. [14] Aleckovic, M., Kang, Y., Regulation of cancer metastasis by cell-free miRNAs. Biochim. Biophys. Acta 2015 (1855), 24–42.
15. [15] Lawrie, C.H., Gal, S., Dunlop, H.M., Pushkaran, B., Liggins, A.P., Pulford, K., et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br. J. Haematol 141 (2008), 672–675.
16. [16] Mitchell, P.S., Parkin, R.K., Kroh, E.M., Fritz, B.R., Wyman, S.K., Pogosova-Agadjanyan, E.L., et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 10513–10518.
17. [17] Abue, M., Yokoyama, M., Shibuya, R., Tamai, K., Yamaguchi, K., Sato, I., et al. Circulating miR-483-3p and miR-21 is highly expressed in plasma of pancreatic cancer. Int. J. Oncol 46 (2015), 539–547.
18. [18] Antolin, S., Calvo, L., Blanco-Calvo, M., Santiago, M.P., Lorenzo-Patino, M.J., Haz-Conde, M., et al. Circulating miR-200c and miR-141 and outcomes in patients with breast cancer. BMC Cancer, 15, 2015, 297.
19. [19] Du, M., Shi, D., Yuan, L., Li, P., Chu, H., Qin, C., et al. Circulating miR-497 and miR-663b in plasma are potential novel biomarkers for bladder cancer. Sci. Rep, 5, 2015, 10437.
20. [20] Lu, Y.C., Chang, J.T., Huang, Y.C., Huang, C.C., Chen, W.H., Lee, L.Y., et al. Combined determination of circulating miR-196a and miR-196b levels produces high sensitivity and specificity for early detection of oral cancer. Clin. Biochem 48 (2015), 115–121.
21. [21] Stuckrath, I., Rack, B., Janni, W., Jager, B., Pantel, K., Schwarzenbach, H., Aberrant plasma levels of circulating miR-16, miR-107, miR-130a and miR-146a are associated with lymph node metastasis and receptor status of breast cancer patients. Oncotarget 6 (2015), 13387–13401.
22. [22] Yu, H., Jiang, L., Sun, C., Li Guo, L., Lin, M., Huang, J., et al. Decreased circulating miR-375: a potential biomarker for patients with non-small-cell lung cancer. Gene 534 (2014), 60–65.
23. [23] Zhang, J., Song, Y., Zhang, C., Zhi, X., Fu, H., Ma, Y., et al. Circulating MiR-16-5p and MiR-19b-3p as two novel potential biomarkers to indicate progression of gastric cancer. Theranostics 5 (2015), 733–745.
24. [24] Shen, J., Hu, Q., Schrauder, M., Yan, L., Wang, D., Medico, L., et al. Circulating miR-148b and miR-133a as biomarkers for breast cancer detection. Oncotarget 5 (2014), 5284–5294.
25. [25] Si, H., Sun, X., Chen, Y., Cao, Y., Chen, S., Wang, H., et al. Circulating microRNA-92a and microRNA-21 as novel minimally invasive biomarkers for primary breast cancer. J. Cancer Res. Clin. Oncol 139 (2013), 223–229.
26. [26] Zhang, L., Zhan, X., Yan, D., Wang, Z., Circulating microRNA-21 is involved in lymph node metastasis in cervical cancer by targeting RASA1. Int. J. Gynecol. Cancer 26 (2016), 810–816.
27. [27] Zhao, S., Yao, D., Chen, J., Ding, N., Circulating miRNA-20a and miRNA-203 for screening lymph node metastasis in early stage cervical cancer. Genet. Test. Mol. Biomarkers 17 (2013), 631–636.
28. [28] Hansen, T.F., Carlsen, A.L., Heegaard, N.H., Sorensen, F.B., Jakobsen, A., Changes in circulating microRNA-126 during treatment with chemotherapy and bevacizumab predicts treatment response in patients with metastatic colorectal cancer. Br. J. Cancer 112 (2015), 624–629.
29. [29] Toiyama, Y., Takahashi, M., Hur, K., Nagasaka, T., Tanaka, K., Inoue, Y., et al. Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer. J. Natl. Cancer Inst 105 (2013), 849–859.
30. [30] Tsujiura, M., Komatsu, S., Ichikawa, D., Shiozaki, A., Konishi, H., Takeshita, H., et al. Circulating miR-18a in plasma contributes to cancer detection and monitoring in patients with gastric cancer. Gastric Cancer 18 (2015), 271–279.
31. [31] Fu, Z., Qian, F., Yang, X., Jiang, H., Chen, Y., Liu, S., Circulating miR-222 in plasma and its potential diagnostic and prognostic value in gastric cancer. Med. Oncol, 31, 2014, 164.
32. [32] Komatsu, S., Ichikawa, D., Tsujiura, M., Konishi, H., Takeshita, H., Nagata, H., et al. Prognostic impact of circulating miR-21 in the plasma of patients with gastric carcinoma. Anticancer Res 33 (2013), 271–276.
33. [33] Koberle, V., Kronenberger, B., Pleli, T., Trojan, J., Imelmann, E., Peveling-Oberhag, J., et al. Serum microRNA-1 and microRNA-122 are prognostic markers in patients with hepatocellular carcinoma. Eur. J. Cancer 49 (2013), 3442–3449.
34. [34] Shen, J., Wang, A., Wang, Q., Gurvich, I., Siegel, A.B., Remotti, H., et al. Exploration of genome-wide circulating microRNA in hepatocellular carcinoma: miR-483-5p as a potential biomarker. Cancer Epidemiol. Biomarkers Prev 22 (2013), 2364–2373.
35. [35] Liu, A.M., Yao, T.J., Wang, W., Wong, K.F., Lee, N.P., Fan, S.T., et al. Circulating miR-15b and miR-130b in serum as potential markers for detecting hepatocellular carcinoma: a retrospective cohort study. BMJ open, 2, 2012 e000825.
36. [36] Takeshita, N., Hoshino, I., Mori, M., Akutsu, Y., Hanari, N., Yoneyama, Y., et al. Serum microRNA expression profile: miR-1246 as a novel diagnostic and prognostic biomarker for oesophageal squamous cell carcinoma. Br. J. Cancer 108 (2013), 644–652.
37. [37] Wang, C., Guan, S., Liu, F., Chen, X., Han, L., Wang, D., et al. Prognostic and diagnostic potential of miR-146a in oesophageal squamous cell carcinoma. Br. J. Cancer 114 (2016), 290–297.
38. [38] Komatsu, S., Ichikawa, D., Hirajima, S., Kawaguchi, T., Miyamae, M., Okajima, W., et al. Plasma microRNA profiles: identification of miR-25 as a novel diagnostic and monitoring biomarker in oesophageal squamous cell carcinoma. Br. J. Cancer 111 (2014), 1614–1624.
39. [39] Morimura, R., Komatsu, S., Ichikawa, D., Takeshita, H., Tsujiura, M., Nagata, H., et al. Novel diagnostic value of circulating miR-18a in plasma of patients with pancreatic cancer. Br. J. Cancer 105 (2011), 1733–1740.
40. [40] Miyamae, M., Komatsu, S., Ichikawa, D., Kawaguchi, T., Hirajima, S., Okajima, W., et al. Plasma microRNA profiles: identification of miR-744 as a novel diagnostic and prognostic biomarker in pancreatic cancer. Br. J. Cancer 113 (2015), 1467–1476.
41. [41] Azizian, A., Kramer, F., Jo, P., Wolff, H.A., Beissbarth, T., Skarupke, R., et al. Preoperative prediction of lymph node status by circulating Mir-18b and Mir-20a during chemoradiotherapy in patients with rectal cancer. World J. Surg 39 (2015), 2329–2335.
42. [42] Cantara, S., Pilli, T., Sebastiani, G., Cevenini, G., Busonero, G., Cardinale, S., et al. Circulating miRNA95 and miRNA190 are sensitive markers for the differential diagnosis of thyroid nodules in a Caucasian population. J. Clin. Endocrinol. Metab 99 (2014), 4190–4198.
43. [43] Lee, J.C., Zhao, J.T., Clifton-Bligh, R.J., Gill, A., Gundara, J.S., Ip, J.C., et al. MicroRNA-222 and microRNA-146b are tissue and circulating biomarkers of recurrent papillary thyroid cancer. Cancer 119 (2013), 4358–4365.
44. [44] Summerer, I., Niyazi, M., Unger, K., Pitea, A., Zangen, V., Hess, J., et al. Changes in circulating microRNAs after radiochemotherapy in head and neck cancer patients. Radiat. Oncol, 8, 2013, 296.
45. [45] Allegra, A., Alonci, A., Campo, S., Penna, G., Petrungaro, A., Gerace, D., et al. Circulating microRNAs: new biomarkers in diagnosis, prognosis and treatment of cancer (review). Int. J. Oncol 41 (2012), 1897–1912.
46. [46] Cui, W., Ma, J., Wang, Y., Biswal, S., Plasma miRNA as biomarkers for assessment of total-body radiation exposure dosimetry. PLoS ONE, 6, 2011 e22988.
47. [47] Chen, G., Wang, J., Cui, Q., Could circulating miRNAs contribute to cancer therapy?. Trends Mol. Med 19 (2013), 71–73.
48. [48] Hanash, S.M., Pitteri, S.J., Faca, V.M., Mining the plasma proteome for cancer biomarkers. Nature 452 (2008), 571–579.
49. [49] Jacob, N.K., Cooley, J.V., Yee, T.N., Jacob, J., Alder, H., Wickramasinghe, P., et al. Identification of sensitive serum microRNA biomarkers for radiation biodosimetry. PLoS ONE, 8, 2013 e57603.
50. [50] Tiberio, P., Callari, M., Angeloni, V., Daidone, M.G., Appierto, V., Challenges in using circulating miRNAs as cancer biomarkers. Biomed Res. Int, 2015, 2015 731479.
51. [51] Leidner, R.S., Li, L., Thompson, C.L., Dampening enthusiasm for circulating microRNA in breast cancer. PLoS ONE, 8, 2013 e57841.
52. [52] Schrauder, M.G., Strick, R., Schulz-Wendtland, R., Strissel, P.L., Kahmann, L., Loehberg, C.R., et al. Circulating micro-RNAs as potential blood-based markers for early stage breast cancer detection. PLoS ONE, 7, 2012 e29770.
53. [53] Margue, C., Reinsbach, S., Philippidou, D., Beaume, N., Walters, C., Schneider, J.G., et al. Comparison of a healthy miRNome with melanoma patient miRNomes: are microRNAs suitable serum biomarkers for cancer?. Oncotarget 6 (2015), 12110–12127.
54. [54] Weber, J.A., Baxter, D.H., Zhang, S., Huang, D.Y., Huang, K.H., Lee, M.J., et al. The microRNA spectrum in 12 body fluids. Clin. Chem 56 (2010), 1733–1741.
55. [55] Becker, N., Lockwood, C.M., Pre-analytical variables in miRNA analysis. Clin. Biochem 46 (2013), 861–868.
56. [56] Farina, N.H., Wood, M.E., Perrapato, S.D., Francklyn, C.S., Stein, G.S., Stein, J.L., et al. Standardizing analysis of circulating microRNA: clinical and biological relevance. J. Cell. Biochem 115 (2014), 805–811.
57. [57] Kosaka, N., Iguchi, H., Ochiya, T., Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101 (2010), 2087–2092.
58. [58] Pritchard, C.C., Cheng, H.H., Tewari, M., MicroRNA profiling: approaches and considerations. Nat. Rev. Genet 13 (2012), 358–369.
59. [59] Pritchard, C.C., Kroh, E., Wood, B., Arroyo, J.D., Dougherty, K.J., Miyaji, M.M., et al. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev. Res. (Phila.) 5 (2012), 492–497.
60. [60] Sourvinou, I.S., Markou, A., Lianidou, E.S., Quantification of circulating miRNAs in plasma: effect of preanalytical and analytical parameters on their isolation and stability. J. Mol. Diagn 15 (2013), 827–834.
61. [61] Wang, K., Yuan, Y., Cho, J.H., McClarty, S., Baxter, D., Galas, D.J., Comparing the microRNA spectrum between serum and plasma. PLoS ONE, 7, 2012 e41561.
62. [62] Turchinovich, A., Weiz, L., Langheinz, A., Burwinkel, B., Characterization of extracellular circulating microRNA. Nucleic Acids Res 39 (2011), 7223–7233.
63. [63] Li, L., Zhu, D., Huang, L., Zhang, J., Bian, Z., Chen, X., et al. Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles. PLoS ONE, 7, 2012 e46957.
64. [64] Zen, K., Zhang, C.Y., Circulating microRNAs: a novel class of biomarkers to diagnose and monitor human cancers. Med. Res. Rev 32 (2012), 326–348.
65. [65] Kroh, E.M., Parkin, R.K., Mitchell, P.S., Tewari, M., Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 50 (2010), 298–301.
66. [66] McDonald, J.S., Milosevic, D., Reddi, H.V., Grebe, S.K., Algeciras-Schimnich, A., Analysis of circulating microRNA: preanalytical and analytical challenges. Clin. Chem 57 (2011), 833–840.
67. [67] Wang, W.T., Chen, Y.Q., Circulating miRNAs in cancer: from detection to therapy. J. Hematol. Oncol, 7, 2014, 86.
68. [68] Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., Wood, M.J., Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol 29 (2011), 341–345.
69. [69] Song, J., Bai, Z., Zhang, J., Meng, H., Cai, J., Deng, W., et al. Serum microRNA-21 levels are related to tumor size in gastric cancer patients but cannot predict prognosis. Oncol. Lett 6 (2013), 1733–1737.
70. [70] Crosbie, P.A., Shah, R., Summers, Y., Dive, C., Blackhall, F., Prognostic and predictive biomarkers in early stage NSCLC: CTCs and serum/plasma markers. Transl. Lung Cancer Res 2 (2013), 382–397.
71. [71] Chen, M., Calin, G.A., Meng, Q.H., Circulating microRNAs as promising tumor biomarkers. Adv. Clin. Chem 67 (2014), 189–214.
72. [72] de Boer, H.C., van Solingen, C., Prins, J., Duijs, J.M., Huisman, M.V., Rabelink, T.J., et al. Aspirin treatment hampers the use of plasma microRNA-126 as a biomarker for the progression of vascular disease. Eur. Heart J. 34 (2013), 3451–3457.
73. [73] Wang, Y.T., Tsai, P.C., Liao, Y.C., Hsu, C.Y., Juo, S.H., Circulating microRNAs have a sex-specific association with metabolic syndrome. J. Biomed. Sci, 20, 2013, 72.
74. [74] Witwer, K.W., XenomiRs and miRNA homeostasis in health and disease: evidence that diet and dietary miRNAs directly and indirectly influence circulating miRNA profiles. RNA Biol 9 (2012), 1147–1154.
75. [75] Willeit, P., Zampetaki, A., Dudek, K., Kaudewitz, D., King, A., Kirkby, N.S., et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ. Res 112 (2013), 595–600.
76. [76] Grasedieck, S., Sorrentino, A., Langer, C., Buske, C., Dohner, H., Mertens, D., et al. Circulating microRNAs in hematological diseases: principles, challenges, and perspectives. Blood 121 (2013), 4977–4984.
77. [77] Bala, S., Petrasek, J., Mundkur, S., Catalano, D., Levin, I., Ward, J., et al. Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 56 (2012), 1946–1957.
78. [78] Yin, W., Zhao, Y., Ji, Y.J., Tong, L.P., Liu, Y., He, S.X., et al. Serum/plasma microRNAs as biomarkers for HBV-related hepatocellular carcinoma in China. Biomed Res. Int, 2015, 2015 965185.
79. [79] Lowery, A.J., Miller, N., McNeill, R.E., Kerin, M.J., MicroRNAs as prognostic indicators and therapeutic targets: potential effect on breast cancer management. Clin. Cancer Res 14 (2008), 360–365.
80. [80] Wulfken, L.M., Moritz, R., Ohlmann, C., Holdenrieder, S., Jung, V., Becker, F., et al. MicroRNAs in renal cell carcinoma: diagnostic implications of serum miR-1233 levels. PLoS ONE, 6, 2011 e25787.
81. [81] Moldovan, L., Batte, K.E., Trgovcich, J., Wisler, J., Marsh, C.B., Piper, M., Methodological challenges in utilizing miRNAs as circulating biomarkers. J. Cell. Mol. Med 18 (2014), 371–390.
82. [82] Zhao, L., Chen, X., Cao, Y., New role of microRNA: carcinogenesis and clinical application in cancer. Acta Biochim. Biophys. Sin. (Shanghai) 43 (2011), 831–839.
83. [83] Boon, R.A., Vickers, K.C., Intercellular transport of microRNAs. Arterioscler. Thromb. Vasc. Biol 33 (2013), 186–192.
84. [84] Vickers, K.C., Palmisano, B.T., Shoucri, B.M., Shamburek, R.D., Remaley, A.T., MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol 13 (2011), 423–433.
85. [85] Chen, X., Ba, Y., Ma, L., Cai, X., Yin, Y., Wang, K., et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18 (2008), 997–1006.
86. [86] Cheng, L., Sharples, R.A., Scicluna, B.J., Hill, A.F., Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J. Extracell. Vesicles, 3, 2014.
87. [87] Cortez, M.A., Bueso-Ramos, C., Ferdin, J., Lopez-Berestein, G., Sood, A.K., Calin, G.A., MicroRNAs in body fluids – the mix of hormones and biomarkers. Nat. Rev. Clin. Oncol 8 (2011), 467–477.
88. [88] Diaz, L.A. Jr., Bardelli, A., Liquid biopsies: genotyping circulating tumor DNA. J. Clin. Oncol 32 (2014), 579–586.
89. [89] Moret, I., Sanchez-Izquierdo, D., Iborra, M., Tortosa, L., Navarro-Puche, A., Nos, P., et al. Assessing an improved protocol for plasma microRNA extraction. PLoS ONE, 8, 2013 e82753.
90. [90] Page, K., Guttery, D.S., Zahra, N., Primrose, L., Elshaw, S.R., Pringle, J.H., et al. Influence of plasma processing on recovery and analysis of circulating nucleic acids. PLoS ONE, 8, 2013 e77963.
91. [91] Baraniskin, A., Kuhnhenn, J., Schlegel, U., Chan, A., Deckert, M., Gold, R., et al. Identification of microRNAs in the cerebrospinal fluid as marker for primary diffuse large B-cell lymphoma of the central nervous system. Blood 117 (2011), 3140–3146.
92. [92] Mall, C., Rocke, D.M., Durbin-Johnson, B., Weiss, R.H., Stability of miRNA in human urine supports its biomarker potential. Biomark. Med 7 (2013), 623–631.
93. [93] Zheng, X.H., Cui, C., Zhou, X.X., Zeng, Y.X., Jia, W.H., Centrifugation: an important pre-analytic procedure that influences plasma microRNA quantification during blood processing. Chin. J. Cancer 32 (2013), 667–672.
94. [94] El-Khoury, V., Pierson, S., Kaoma, T., Bernardin, F., Berchem, G., Assessing cellular and circulating miRNA recovery: the impact of the RNA isolation method and the quantity of input material. Sci. Rep, 6, 2016, 19529.
95. [95] Ono, S., Lam, S., Nagahara, M., Hoon, D.S., Circulating microRNA biomarkers as liquid biopsy for cancer patients: pros and cons of current assays. J. Clin. Med 4 (2015), 1890–1907.
96. [96] Thery, C., Zitvogel, L., Amigorena, S., Exosomes: composition, biogenesis and function. Nat. Rev. Immunol 2 (2002), 569–579.
97. [97] Williams, Z., Ben-Dov, I.Z., Elias, R., Mihailovic, A., Brown, M., Rosenwaks, Z., et al. Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 4255–4260.
98. [98] O'Driscoll, L., Extracellular nucleic acids and their potential as diagnostic, prognostic and predictive biomarkers. Anticancer Res 27 (2007), 1257–1265.
99. [99] Zampetaki, A., Mayr, M., Analytical challenges and technical limitations in assessing circulating miRNAs. Thromb. Haemost 108 (2012), 592–598.
100. [100] 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 24 (2013), 542–556.
101. [101] Tsochandaridis, M., Nasca, L., Toga, C., Levy-Mozziconacci, A., Circulating microRNAs as clinical biomarkers in the predictions of pregnancy complications. Biomed Res. Int, 2015, 2015 294954.
102. [102] Ward, J., Kanchagar, C., Veksler-Lublinsky, I., Lee, R.C., McGill, M.R., Jaeschke, H., et al. Circulating microRNA profiles in human patients with acetaminophen hepatotoxicity or ischemic hepatitis. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 12169–12174.
103. [103] Khalyfa, A., Gozal, D., Exosomal miRNAs as potential biomarkers of cardiovascular risk in children. J. Transl. Med, 12, 2014, 162.
104. [104] Hu, Z., Chen, X., Zhao, Y., Tian, T., Jin, G., Shu, Y., et al. Serum microRNA signatures identified in a genome-wide serum microRNA expression profiling predict survival of non-small-cell lung cancer. J. Clin. Oncol 28 (2010), 1721–1726.
105. [105] Haider, B.A., Baras, A.S., McCall, M.N., Hertel, J.A., Cornish, T.C., Halushka, M.K., A critical evaluation of microRNA biomarkers in non-neoplastic disease. PLoS ONE, 9, 2014 e89565.
106. [106] Wang, M., Gu, H., Wang, S., Qian, H., Zhu, W., Zhang, L., et al. Circulating miR-17-5p and miR-20a: molecular markers for gastric cancer. Mol. Med. Rep 5 (2012), 1514–1520.
107. [107] Wang, B., Zhang, Q., The expression and clinical significance of circulating microRNA-21 in serum of five solid tumors. J. Cancer Res. Clin. Oncol 138 (2012), 1659–1666.
108. [108] Valladares-Ayerbes, M., Reboredo, M., Medina-Villaamil, V., Iglesias-Diaz, P., Lorenzo-Patino, M.J., Haz, M., et al. Circulating miR-200c as a diagnostic and prognostic biomarker for gastric cancer. J. Transl. Med, 10, 2012, 186.
109. [109] Shalaby, T., Fiaschetti, G., Baumgartner, M., Grotzer, M.A., MicroRNA signatures as biomarkers and therapeutic target for CNS embryonal tumors: the pros and the cons. Int. J. Mol. Sci 15 (2014), 21554–21586.
110. [110] Yang, M., Chen, J., Su, F., Yu, B., Su, F., Lin, L., et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol. Cancer, 10, 2011, 117.
111. [111] Ho, S.L., Chan, H.M., Wong, R.N., Li, H.W., Self-assembling protein platform for direct quantification of circulating microRNAs in serum with total internal reflection fluorescence microscopy. Anal. Chim. Acta 823 (2014), 61–68.
112. [112] Labib, M., Berezovski, M.V., Electrochemical sensing of microRNAs: avenues and paradigms. Biosens. Bioelectron 68 (2015), 83–94.
113. [113] Lusi, E.A., Passamano, M., Guarascio, P., Scarpa, A., Schiavo, L., Innovative electrochemical approach for an early detection of microRNAs. Anal. Chem 81 (2009), 2819–2822.
114. [114] Zhao, H., Shen, J., Medico, L., Wang, D., Ambrosone, C.B., Liu, S., A pilot study of circulating miRNAs as potential biomarkers of early stage breast cancer. PLoS ONE, 5, 2010 e13735.