Small RNAs have a large impact: Circulating microRNAs as biomarkers for human diseases

RNA Biology

Volumn 9, Issue 6, 2012, Pages 850-859

  Weiland, Matthew ^a   Gao, Xing Hua ^b   Zhou, Li ^a   Mi, Qing Sheng ^a  

^a HENRY FORD HEALTH SYSTEM   (United States)

^b CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Biomarker; Circulating; MicroRNA

Indexed keywords

DNA; MICRORNA; MICRORNA 103; MICRORNA 107; MICRORNA 141; MICRORNA 155; MICRORNA 16; MICRORNA 195; MICRORNA 196A; MICRORNA 197; MICRORNA 200A; MICRORNA 200B; MICRORNA 21; MICRORNA 210; MICRORNA 328; MICRORNA 34B; MICRORNA 375; MICRORNA 485 3P; MICRORNA 486 5P; MICRORNA 574 3P; MICRORNA 636; MICRORNA 638; MICRORNA 640; MICRORNA 766; MICRORNA 885 5P; MICRORNA 92; MICRORNA 92A; MICRORNA 92B; MICRORNA 93; TUMOR MARKER; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE HEART INFARCTION; B CELL LEUKEMIA; B CELL LYMPHOMA; BIPOLAR MANIA; BREAST CANCER; CANCER CELL; CANCER DIAGNOSIS; CANCER PROGNOSIS; CARCINOGENESIS; CARDIOVASCULAR DISEASE; CELL FREE SYSTEM; CELL PROLIFERATION; COLORECTAL CANCER; DIAGNOSTIC VALUE; EARLY DIAGNOSIS; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HEART INJURY; HUMAN; INFECTION; LARGE CELL LYMPHOMA; LIVER INJURY; LUNG NON SMALL CELL CANCER; MELANOMA; MENTAL DISEASE; MOUTH SQUAMOUS CELL CARCINOMA; OVARY CANCER; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PREDICTIVE VALUE; PREGNANCY; PROSTATE CANCER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SENSITIVITY AND SPECIFICITY; SQUAMOUS CELL CARCINOMA; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; STOMACH CANCER;

EID: 84863425849     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.20378     Document Type: Review

References (61)

1. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75:843-54; PMID:8252621; http://dx.doi.org/10.1016/0092-8674(93)90529-Y.
2. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136:215-33; PMID:19167326; http://dx.doi.org/10.1016/j.cell.2009.01.002.
3. Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000; 408:86-9; PMID:11081512; http://dx.doi.org/10.1038/35040556.
4. Cobb BS, Nesterova TB, Thompson E, Hertweck A, O'Connor E, Godwin J, et al. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J Exp Med 2005; 201:1367-73; PMID:15867090; http://dx.doi.org/10. 1084/jem.20050572.
5. Harfe BD, McManus MT, Mansfield JH, Hornstein E, Tabin CJ. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci USA 2005; 102:10898-903; PMID:16040801; http://dx.doi.org/10.1073/pnas.0504834102.
6. Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, Zhao G. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 2005; 280:9330-5; PMID:15613470; http://dx.doi.org/10.1074/jbc.M413394200.
7. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, et al. Frequent deletions and downregulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99:15524-9; PMID:12434020; http://dx.doi.org/10.1073/pnas.242606799.
8. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006; 6:857-66; PMID:17060945; http://dx.doi.org/10.1038/nrc1997.
9. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006; 6:259-69; PMID:16557279; http://dx.doi.org/10.1038/ nrc1840.
10. Mandel P, Metais P. Les acides necleiques du plasma sanguin chez l'Homme. C R Acad Sci Paris 1948; 142:241-3.
11. Ayala W, Moore LV, Hess EL. The purple color reaction given by diphenylamine reagent. I. With normal and rheumatic fever sera. J Clin Invest 1951; 30:781-5; PMID:14850558; http://dx.doi.org/10.1172/JCI102492.
12. Leon SA, Shapiro B, Sklaroff DM, Yaros MJ. Free DNA in the serum of cancer patients and the effect of therapy. Cancer Res 1977; 37:646-50; PMID:837366.
13. Tong YK, Lo YM. Diagnostic developments involving cell-free (circulating) nucleic acids. Clin Chim Acta 2006; 363:187-96; PMID:16126188; http://dx.doi.org/10.1016/j.cccn.2005.05.048.
14. Stroun M, Anker P, Maurice P, Lyautey J, Lederrey C, Beljanski M. Neoplastic characteristics of the DNA found in the plasma of cancer patients. Oncology 1989; 46:318-22; PMID:2779946; http://dx.doi.org/10.1159/000226740.
15. 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 2008; 18:997-1006; PMID:18766170; http://dx.doi.org/10. 1038/cr.2008.282.
16. Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, et al. Serum microRNAs are promising novel biomarkers. PLoS One 2008; 3:3148; PMID:18773077; http://dx.doi.org/10.1371/journal.pone.0003148.
17. Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, 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 2008; 141:672-5; PMID:18318758; http://dx.doi.org/10.1111/j.1365-2141.2008.07077.x.
18. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105:10513-8; PMID:18663219; http://dx.doi.org/10.1073/pnas.0804549105.
19. Wang K, Zhang S, Marzolf B, Troisch P, Brightman A, Hu Z, et al. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA 2009; 106:4402-7; PMID:19246379; http://dx.doi.org/10.1073/ pnas.0813371106.
20. Lodes MJ, Caraballo M, Suciu D, Munro S, Kumar A, Anderson B. Detection of cancer with serum miRNAs on an oligonucleotide microarray. PLoS One 2009; 4:6229; PMID:19597549; http://dx.doi.org/10.1371/journal.pone.0006229.
21. Brase JC, Johannes M, Schlomm T, Fälth M, Haese A, Steuber T, et al. Circulating miRNAs are correlated with tumor progression in prostate cancer. Int J Cancer 2011; 128:608-16; PMID:20473869; http://dx.doi.org/10.1002/ijc. 25376.
22. Tanaka M, Oikawa K, Takanashi M, Kudo M, Ohyashiki J, Ohyashiki K, et al. Downregulation of miR-92 in human plasma is a novel marker for acute leukemia patients. PLoS One 2009; 4:5532; PMID:19440243; http://dx.doi.org/10.1371/ journal.pone.0005532.
23. Wang J, Chen J, Chang P, LeBlanc A, Li D, Abbruzzesse JL, et al. MicroRNAs in plasma of pancreatic ductal adenocarcinoma patients as novel blood-based biomarkers of disease. [Phila Pa]. Cancer Prev Res (Phila) 2009; 2:807-13; PMID:19723895; http://dx.doi.org/10.1158/1940-6207.CAPR-09-0094.
24. Ho AS, Huang X, Cao H, Christman-Skieller C, Bennewith K, Le QT, et al. Circulating miR-210 as a Novel Hypoxia Marker in Pancreatic Cancer. Transl Oncol 2010; 3:109-13; PMID:20360935.
25. Kong X, Du Y, Wang G, Gao J, Gong Y, Li L, et al. Detection of differentially expressed microRNAs in serum of pancreatic ductal adenocarcinoma patients: miR-196a could be a potential marker for poor prognosis. Dig Dis Sci 2011; 56:602-9; PMID:20614181; http://dx.doi.org/10.1007/s10620-010-1285-3.
26. Li A, Omura N, Hong SM, Vincent A, Walter K, Griffith M, et al. Pancreatic cancers epigenetically silence SIP1 and hypomethylate and overexpress miR-200a/200b in association with elevated circulating miR-200a and miR-200b levels. Cancer Res 2010; 70:5226-37; PMID:20551052; http://dx.doi.org/10.1158/ 0008-5472.CAN-09-4227.
27. Resnick KE, Alder H, Hagan JP, Richardson DL, Croce CM, Cohn DE. The detection of differentially expressed microRNAs from the serum of ovarian cancer patients using a novel real-time PCR platform. Gynecol Oncol 2009; 112:55-9; PMID:18954897; http://dx.doi.org/10.1016/j.ygyno.2008.08.036.
28. Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Newell J, Kerin MJ. Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann Surg 2010; 251:499-505; PMID:20134314; http://dx.doi.org/10.1097/SLA. 0b013e3181cc939f.
29. Zhu W, Qin W, Atasoy U, Sauter ER. Circulating microRNAs in breast cancer and healthy subjects. BMC Res Notes 2009; 2:89; PMID:19454029; http://dx.doi.org/10.1186/1756-0500-2-89.
30. Roth C, Rack B, Müller 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; 12:90; PMID:21047409; http://dx.doi.org/10.1186/bcr2766.
31. Asaga S, Kuo C, Nguyen T, Terpenning M, Giuliano AE, Hoon DS. Direct serum assay for microRNA-21 concentrations in early and advanced breast cancer. Clin Chem 2011; 57:84-91; PMID:21036945; http://dx.doi.org/10.1373/clinchem. 2010.151845.
32. Ng EK, Chong WW, Jin H, Lam EK, Shin VY, Yu J, et al. Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut 2009; 58:1375-81; PMID:19201770; http://dx.doi.org/10.1136/gut.2008.167817.
33. Huang Z, Huang D, Ni S, Peng Z, Sheng W, Du X. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int J Cancer 2010; 127:118-26; PMID:19876917; http://dx.doi.org/10.1002/ijc.25007.
34. Tsujiura M, Ichikawa D, Komatsu S, Shiozaki A, Takeshita H, Kosuga T, et al. Circulating microRNAs in plasma of patients with gastric cancers. Br J Cancer 2010; 102:1174-9; PMID:20234369; http://dx.doi.org/10.1038/sj.bjc. 6605608.
35. Liu R, Zhang C, Hu Z, Li G, Wang C, Yang C, et al. A five-microRNA signature identified from genome-wide serum microRNA expression profiling serves as a fingerprint for gastric cancer diagnosis. Eur J Cancer 2011; 47:784-91; PMID:21112772; http://dx.doi.org/10.1016/j.ejca.2010.10.025.
36. Wong TS, Liu XB, Wong BY, Ng RW, Yuen AP, Wei WI. Mature miR-184 as Potential Oncogenic microRNA of Squamous Cell Carcinoma of Tongue. Clin Cancer Res 2008; 14:2588-92; PMID:18451220; http://dx.doi.org/10.1158/1078-0432.CCR-07- 0666.
37. Lin SC, Liu CJ, Lin JA, Chiang WF, Hung PS, Chang KW. miR-24 upregulation in oral carcinoma: positive association from clinical and in vitro analysis. Oral Oncol 2010; 46:204-8; PMID:20138800; http://dx.doi.org/10.1016/j. oraloncology.2009.12.005.
38. Liu CJ, Kao SY, Tu HF, Tsai MM, Chang KW, Lin SC. Increase of microRNA miR-31 level in plasma could be a potential marker of oral cancer. Oral Dis 2010; 16:360-4; PMID:20233326; http://dx.doi.org/10.1111/j.1601-0825.2009.01646. x.
39. Zhang C, Wang C, Chen X, Yang C, Li K, Wang J, et al. Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin Chem 2010; 56:1871-9; PMID:20943850; http://dx.doi.org/10.1373/clinchem. 2010.147553.
40. Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Morimura R, Nagata H, et al. Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer 2011; 105:104-11; PMID:21673684; http://dx.doi.org/10. 1038/bjc.2011.198.
41. 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 2010; 28:1721-6; PMID:20194856; http://dx.doi.org/10.1200/JCO.2009.24.9342.
42. Foss KM, Sima C, Ugolini D, Neri M, Allen KE, Weiss GJ. miR-1254 and miR-574-5p: serum-based microRNA biomarkers for early-stage non-small cell lung cancer. J Thorac Oncol 2011; 6:482-8; PMID:21258252; http://dx.doi.org/10.1097/ JTO.0b013e318208c785.
43. Liu XG, Zhu WY, Huang YY, Ma LN, Zhou SQ, Wang YK, et al. High expression of serum miR-21 and tumor miR-200c associated with poor prognosis in patients with lung cancer. Med Oncol 2011; PMID:21516486; http://dx.doi.org/10.1007/ s12032-011-9923-y.
44. Wei J, Gao W, Zhu CJ, Liu YQ, Mei Z, Cheng T, et al. Identification of plasma microRNA-21 as a biomarker for early detection and chemosensitivity of non-small cell lung cancer. Chin J Cancer 2011; 30:407-14; PMID:21627863; http://dx.doi.org/10.5732/cjc.010.10522.
45. Kanemaru H, Fukushima S, Yamashita J, Honda N, Oyama R, Kakimoto A, et al. The circulating microRNA-221 level in patients with malignant melanoma as a new tumor marker. J Dermatol Sci 2011; 61:187-93; PMID:21273047; http://dx.doi.org/10.1016/j.jdermsci.2010.12.010.
46. Ji X, Takahashi R, Hiura Y, Hirokawa G, Fukushima Y, Iwai N. Plasma miR-208 as a biomarker of myocardial injury. Clin Chem 2009; 55:1944-9; PMID:19696117; http://dx.doi.org/10.1373/clinchem.2009.125310.
47. Wang GK, Zhu JQ, Zhang JT, Li Q, Li Y, He J, et al. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J 2010; 31:659-66; PMID:20159880; http://dx.doi.org/10. 1093/eurheartj/ehq013.
48. Cheng Y, Tan N, Yang J, Liu X, Cao X, He P, et al. A translational study of circulating cell-free microRNA-1 in acute myocardial infarction. Clin Sci (Lond) 2010; 119:87-95; PMID:20218970; http://dx.doi.org/10.1042/CS20090645.
49. Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, et al. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun 2010; 391:73-7; PMID:19896465; http://dx.doi.org/10.1016/j.bbrc.2009. 11.005.
50. D'Alessandra Y, Devanna P, Limana F, Straino S, Di Carlo A, Brambilla PG, et al. Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur Heart J 2010; 31:2765-73; PMID:20534597; http://dx.doi.org/10. 1093/eurheartj/ehq167.
51. Tijsen AJ, Creemers EE, Moerland PD, de Windt LJ, van der Wal AC, Kok WE, et al. MiR423-5p as a circulating biomarker for heart failure. Circ Res 2010; 106:1035-9; PMID:20185794; http://dx.doi.org/10.1161/CIRCRESAHA.110.218297.
52. Laterza OF, Lim L, Garrett-Engele PW, Vlasakova K, Muniappa N, Tanaka WK, et al. Plasma MicroRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem 2009; 55:1977-83; PMID:19745058; http://dx.doi.org/10.1373/clinchem. 2009.131797.
53. 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; 4:7405; PMID:19823581; http://dx.doi.org/10.1371/ journal.pone.0007405.
54. Wang JF, Yu ML, Yu G, Bian JJ, Deng XM, Wan XJ, et al. Serum miR-146a and miR-223 as potential new biomarkers for sepsis. Biochem Biophys Res Commun 2010; 394:184-8; PMID:20188071; http://dx.doi.org/10.1016/j.bbrc.2010.02.145.
55. Rong H, Liu TB, Yang KJ, Yang HC, Wu DH, Liao CP, et al. MicroRNA-134 plasma levels before and after treatment for bipolar mania. J Psychiatr Res 2011; 45:92-5; PMID:20546789; http://dx.doi.org/10.1016/j.jpsychires.2010.04. 028.
56. Starkey Lewis PJ, Dear J, Platt V, Simpson KJ, Craig DG, Antoine DJ, et al. Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology 2011; 54:1767-76; PMID:22045675; http://dx.doi.org/10.1002/ hep.24538.
57. Wang G, Tam LS, Li EK, Kwan BC, Chow KM, Luk CC, et al. Serum and urinary free microRNA level in patients with systemic lupus erythematosus. Lupus 2011; 20:493-500; PMID:21372198; http://dx.doi.org/10.1177/0961203310389841.
58. Qi R, Weiland M, Gao XX, Zhou L, Mi QS. Identification of endogenous normalizers for serum miRNAs by microarray profiling: U6 snRNA is not a reliable normalizer. Hepatology 2011; PMID:22213067; http://dx.doi.org/10.1002/hep. 25558.
59. Smalheiser NR. Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol Direct 2007; 2:35; PMID:18053135; http://dx.doi.org/10. 1186/1745-6150-2-35.
60. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10:1470-6; PMID:19011622; http://dx.doi.org/10.1038/ncb1800.
61. Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA. MicroRNAs in body fluids - the mix of hormones and biomarkers. Nat Rev Clin Oncol 2011; 8:467-77; PMID:21647195; http://dx.doi.org/10.1038/nrclinonc.2011. 76.