Cell-free microRNAs as cancer biomarkers: the odyssey of miRNAs through body fluids

Medical Oncology

Volumn 31, Issue 12, 2014, Pages 1-11

  Javidi, Mohammad Amin ^a   Ahmadi, Amir Hossein ^a   Bakhshinejad, Babak ^a   Nouraee, Nazila ^a   Babashah, Sadegh ^a   Sadeghizadeh, Majid ^a  

^a TARBIAT MODARES UNIVERSITY   (Iran)

Author keywords

Cancer biomarker; Cell free microRNA; Detection; Diagnosis; Exosome; Extracellular miRNA; Secretory miRNA

Indexed keywords

ARGONAUTE 2 PROTEIN; CARCINOEMBRYONIC ANTIGEN; CELL FREE MICRORNA; ESCRT PROTEIN; HIGH DENSITY LIPOPROTEIN; MICRORNA; MICRORNA 106A; MICRORNA 106B; MICRORNA 124 3P; MICRORNA 142 3P; MICRORNA 150; MICRORNA 155; MICRORNA 16; MICRORNA 17 3P; MICRORNA 17 5P; MICRORNA 195; MICRORNA 21; MICRORNA 222; MICRORNA 29A; MICRORNA 30C 5P; MICRORNA 638; MICRORNA 92; NUCLEOPHOSMIN; PROSTATE SPECIFIC ANTIGEN; RNA BINDING PROTEIN; TUMOR MARKER; UNCLASSIFIED DRUG;

BODY FLUID; BREAST CANCER; CANCER SURVIVAL; CELL COMMUNICATION; CELL DEATH; CELL MIGRATION; CEREBROSPINAL FLUID; CHRONIC LYMPHATIC LEUKEMIA; COLORECTAL CANCER; CYTOPLASM; CYTOSKELETON; ENDOSOME; EXOSOME; EXTRACELLULAR SPACE; GLIOBLASTOMA; HIGH THROUGHPUT SCREENING; HUMAN; LARGE CELL LYMPHOMA; LIVER CELL CARCINOMA; LUNG CANCER; MICROARRAY ANALYSIS; MOUTH SQUAMOUS CELL CARCINOMA; MULTIVESICULAR BODY; NEXT GENERATION SEQUENCING; OVARY CANCER; OVERALL SURVIVAL; PANCREAS CANCER; PROSTATE CANCER; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RECURRENCE FREE SURVIVAL; REVIEW; RHABDOMYOSARCOMA; SENSITIVITY AND SPECIFICITY; STOMACH CANCER; ANIMAL; CELL MEMBRANE; CHEMISTRY; METABOLISM; NEOPLASMS;

ANIMALS; BODY FLUIDS; CELL MEMBRANE; HUMANS; MICRORNAS; NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84919916427     PISSN: 13570560     EISSN: 1559131X     Source Type: Journal    
DOI: 10.1007/s12032-014-0295-y     Document Type: Review

References (92)

1. Babashah S, Soleimani M. The oncogenic and tumour suppressive roles of microRNAs in cancer and apoptosis. Eur J Cancer. 2011;47:1127–37.
2. Babashah S, Sadeghizadeh M, Tavirani MR, Farivar S, Soleimani M. Aberrant microRNA expression and its implications in the pathogenesis of leukemias. Cell Oncol (Dordr). 2012;35:317–34.
3. Babashah S. editor, MicroRNAs: key regulators of oncogenesis. Switzerland: Springer International Publishing; 2014. p. 3–28.
4. Lynam-Lennon N, Maher SG, Reynolds JV. The roles of microRNA in cancer and apoptosis. Biol Rev Camb Philos Soc. 2009;84:55–71.
5. Chim SSC, Shing TKF, Hung ECW, et al. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem. 2008;54:482–90.
6. Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci. 2008;105:10513–8.
7. Park NJ, Zhou H, Elashoff D, et al. Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin Cancer Res. 2009;15:5473–7.
8. Chen X, Gao C, Li H, et al. Identification and characterization of microRNAs in raw milk during different periods of lactation, commercial fluid, and powdered milk products. Cell Res. 2010;20:1128–37.
9. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285:17442–52.
10. Kato, Y. An efficient fluorescent method for selective detection of mature miRNA species. In: Nucleic Acids Symposium Series. Oxford University Press; 2008. p. 71–72.
11. Roy S, Soh JH, Gao Z. A microfluidic-assisted microarray for ultrasensitive detection of miRNA under an optical microscope. Lab Chip. 2011;11:1886–94.
12. Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 2010;38:7248–59.
13. Zernecke A, Bidzhekov K, Noels H, et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal. 2009;2:ra81.
14. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13:423–33.
15. Zhang J, Zhao H, Gao Y, Zhang W. Secretory miRNAs as novel cancer biomarkers. Biochim Biophys Acta. 2012;1826:32–43.
16. Zhang Q, Xu J, Chen Q, Chen X, Zen K, Zhang C-Y. Selective secretion of microRNA in CNS system. Protein Cell. 2013;4:243–7.
17. Turchinovich A, Weiz L, Burwinkel B. Extracellular miRNAs: the mystery of their origin and function. Trends Biochem Sci. 2012;37:460–5.
18. Turchinovich A, et al. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39:7223–33.
19. Simons M, Raposo G. Exosomes–vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009;21:575–81.
20. 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.
21. Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–79.
22. Ronquist G, Brody I. The prostasome: its secretion and function in man. Biochim Biophys Acta. 1985;822:203–18.
23. Tetta C, Ghigo E, Silengo L, Deregibus MC, Camussi G. Extracellular vesicles as an emerging mechanism of cell-to-cell communication. Endocrine. 2013;44:11–9.
24. Weber JA, Baxter DH, Zhang S, et al. The microRNA spectrum in 12 body fluids. Clin Chem. 2010;56:1733–41.
25. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19:43–51.
26. Yuan A, Farber EL, Rapoport AL, et al. Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One. 2009;4:e4722.
27. Collino F, Deregibus MC, Bruno S, et al. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One. 2010;5:e11803.
28. Zhang Y, Liu D, Chen X, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133–44.
29. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009;11:1143–9.
30. Trajkovic K, Hsu C, Chiantia S, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319:1244–7.
31. Fabbri M, Paone A, Calore F, et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA. 2012;109:E2110–6.
32. Chen X, Liang H, Zhang J, Zen K, Zhang C-Y. Horizontal transfer of microRNAs: molecular mechanisms and clinical applications. Protein Cell. 2012;3:28–37.
33. Kosaka N, Ochiya T. Unraveling the mystery of cancer by secretory microRNA: horizontal microRNA transfer between living cells. Front Genet. 2012;2:97.
34. Atay S, Gercel-Taylor C, Kesimer M, Taylor DD. Morphologic and proteomic characterization of exosomes released by cultured extravillous trophoblast cells. Exp Cell Res. 2011;317:1192–202.
35. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.
36. Sahoo S, Losordo DW. Exosomes and cardiac repair after myocardial infarction. Circ Res. 2014;114:333–44.
37. Bang C, Batkai S, Dangwal S, et al. Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest. 2014;124:2136–46.
38. Ludwig JA, Weinstein JN. Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev Cancer. 2005;5:845–56.
39. Mulrane L, Klinger R, McGee SF, Gallagher WM, O’Connor DP. microRNAs: a new class of breast cancer biomarkers. Expert Rev Mol Diagn. 2014;14:347–63.
40. Etheridge A, Lee I, Hood L, Galas D, Wang K. Extracellular microRNA: a new source of biomarkers. Mutat Res. 2011;717:85–90.
41. 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.
42. 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.
43. Lawrie CH, Gal S, Dunlop HM, 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.
44. Moussay E, Wang K, Cho J-H, et al. MicroRNA as biomarkers and regulators in B-cell chronic lymphocytic leukemia. Proc Natl Acad Sci. 2011;108:6573–8.
45. Wu Q, Lu Z, Li H, Lu J, Guo L, Ge Q. Next-generation sequencing of microRNAs for breast cancer detection. J Biomed Biotechnol. 2011;2011:597145.
46. Zhu W, Qin W, Atasoy U, Sauter ER. Circulating microRNAs in breast cancer and healthy subjects. BMC Res Notes. 2009;2:89.
47. Ng EKO, Chong WWS, Jin H, 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.
48. Tsujiura M, Ichikawa D, Komatsu S, et al. Circulating microRNAs in plasma of patients with gastric cancers. Br J Cancer. 2010;102:1174–9.
49. Berindan-Neagoe I, Monroig Pdel C, Pasculli B, Calin GA. MicroRNAome genome: a treasure for cancer diagnosis and therapy. CA Cancer J Clin. 2014;64:311–36.
50. de Planell-Saguer M, Rodicio MC. Analytical aspects of microRNA in diagnostics: a review. Anal Chim Acta. 2011;699:134–52.
51. Van Roosbroeck K, Pollet J, Calin GA. miRNAs and long noncoding RNAs as biomarkers in human diseases. Expert Rev Mol Diagn. 2013;13:183–204.
52. Havelda Z. In situ detection of miRNAs using LNA probes. Methods Mol Biol. 2010;592:127–36.
53. Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet. 2012;13:358–69.
54. Love C, Dave S. MicroRNA expression profiling using microarrays. Methods Mol Biol. 2013;999:285–96.
55. 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.
56. Qu KZ, Zhang K, Li H, Afdhal NH, Albitar M. Circulating microRNAs as biomarkers for hepatocellular carcinoma. J Clin Gastroenterol. 2011;45:355–60.
57. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–9.
58. Heneghan HM, Miller N, Kelly R, Newell J, Kerin MJ. Systemic miRNA-195 differentiates breast cancer from other malignancies and is a potential biomarker for detecting noninvasive and early stage disease. Oncologist. 2010;15:673–82.
59. Xie L, Chen X, Wang L, et al. Cell-free miRNAs may indicate diagnosis and docetaxel sensitivity of tumor cells in malignant effusions. BMC Cancer. 2010;10:591.
60. Liu R, Zhang C, Hu Z, 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.
61. 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.
62. Cheng H, Zhang L, Cogdell DE, et al. Circulating plasma MiR-141 is a novel biomarker for metastatic colon cancer and predicts poor prognosis. PLoS One. 2011;6:e17745.
63. Hu Z, Chen X, Zhao 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.
64. Silva J, García V, Zaballos A, et al. Vesicle-related microRNAs in plasma of nonsmall cell lung cancer patients and correlation with survival. Eur Respir J. 2011;37:617–23.
65. Liu X-G, Zhu W-Y, Huang Y-Y, et al. High expression of serum miR-21 and tumor miR-200c associated with poor prognosis in patients with lung cancer. Med Oncol. 2012;29:618–26.
66. Wang ZX, Bian HB, Wang JR, Cheng ZX, Wang KM, De W. Prognostic significance of serum miRNA-21 expression in human non-small cell lung cancer. J Surg Oncol. 2011;104:847–51.
67. 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.
68. Shen J, Liu Z, Todd NW, et al. Diagnosis of lung cancer in individuals with solitary pulmonary nodules by plasma microRNA biomarkers. BMC Cancer. 2011;11:374.
69. Shen J, Todd NW, Zhang H, et al. Plasma microRNAs as potential biomarkers for non-small-cell lung cancer. Lab Invest. 2011;91:579–87.
70. Tanaka M, Oikawa K, Takanashi M, et al. Down-regulation of miR-92 in human plasma is a novel marker for acute leukemia patients. PLoS One. 2009;4:e5532.
71. Guo H-Q, Huang G-L, Guo C-C, Pu X-X, Lin T-Y. Diagnostic and prognostic value of circulating miR-221 for extranodal natural killer/T-cell lymphoma. Dis Markers. 2010;29:251–8.
72. Brase JC, Johannes M, Schlomm T, et al. Circulating miRNAs are correlated with tumor progression in prostate cancer. Int J Cancer. 2011;128:608–16.
73. Yaman Agaoglu F, Kovancilar M, Dizdar Y, et al. Investigation of miR-21, miR-141, and miR-221 in blood circulation of patients with prostate cancer. Tumour Biol. 2011;32:583–8.
74. Gui J, Tian Y, Wen X, et al. Serum microRNA characterization identifies miR-885-5p as a potential marker for detecting liver pathologies. Clin Sci (Lond). 2011;120:183–93.
75. Li J, Wang Y, Yu W, Chen J, Luo J. Expression of serum miR-221 in human hepatocellular carcinoma and its prognostic significance. Biochem Biophys Res Commun. 2011;406:70–3.
76. Xu J, Wu C, Che X, et al. Circulating microRNAs, miR-21, miR-122, and miR-223, in patients with hepatocellular carcinoma or chronic hepatitis. Mol Carcinog. 2011;50:136–42.
77. Yamamoto Y, Kosaka N, Tanaka M, et al. MicroRNA-500 as a potential diagnostic marker for hepatocellular carcinoma. Biomarkers. 2009;14:529–38.
78. Li L-M, Hu Z-B, Zhou Z-X, et al. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res. 2010;70:9798–807.
79. Wang J, Chen J, Chang P, et al. MicroRNAs in plasma of pancreatic ductal adenocarcinoma patients as novel blood-based biomarkers of disease. Cancer Prev Res (Phila). 2009;2:807–13.
80. 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.
81. Miyachi M, Tsuchiya K, Yoshida H, et al. Circulating muscle-specific microRNA, miR-206, as a potential diagnostic marker for rhabdomyosarcoma. Biochem Biophys Res Commun. 2010;400:89–93.
82. 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.
83. 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.
84. Momen-Heravi F, Trachtenberg AJ, Kuo WP, Cheng YS. Genomewide study of salivary MicroRNAs for detection of oral cancer. J Dent Res. 2014;93:86S–93S.
85. Wu W, Hou W, Wu Z, Wang Y, Yi Y, Lin W. [miRNA-144 in the saliva is a genetic marker for early diagnosis of esophageal cancer]. Nan Fang Yi Ke Da Xue Xue Bao. 2013;33:1783–6.
86. Liu CJ, Lin SC, Yang CC, Cheng HW, Chang KW. Exploiting salivary miR-31 as a clinical biomarker of oral squamous cell carcinoma. Head Neck. 2012;34:219–24.
87. Hanke M, Hoefig K, Merz H, et al. A robust methodology to study urine microRNA as tumor marker: microRNA-126 and microRNA-182 are related to urinary bladder cancer. Urol Oncol. 2010;28:655–61.
88. Abdalla MA, Haj-Ahmad Y. Promising candidate urinary MicroRNA biomarkers for the early detection of hepatocellular carcinoma among high-risk Hepatitis C virus Egyptian patients. J Cancer. 2012;3:19–31.
89. Srivastava A, Goldberger H, Dimtchev A, et al. MicroRNA profiling in prostate cancer–the diagnostic potential of urinary miR-205 and miR-214. PLoS One. 2013;8:e76994.
90. Bryant RJ, Pawlowski T, Catto JW, et al. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer. 2012;106:768–74.
91. Corcoran C, Rani S, O’Driscoll L. miR-34a is an intracellular and exosomal predictive biomarker for response to docetaxel with clinical relevance to prostate cancer progression. Prostate. 2014;74:1320–34.
92. Zhang DZ, Lau KM, Chan ES, et al. Cell-free urinary microRNA-99a and microRNA-125b are diagnostic markers for the non-invasive screening of bladder cancer. PLoS One. 2014;9:e100793.