Circulating microRNAs: New biomarkers in diagnosis, prognosis and treatment of cancer (Review)

International Journal of Oncology

Volumn 41, Issue 6, 2012, Pages 1897-1912

  Allegra, Alessandro ^a   Alonci, Andrea ^a   Campo, Salvatore ^b   Penna, Giuseppa ^a   Petrungaro, Annamaria ^a   Gerace, Demetrio ^a   Musolino, Caterina ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF MESSINA   (Italy)

Author keywords

Cancer; Cellular microRNAs; Circulating microRNAs; Extracellular communication RNAs; Gene expression; Non coding RNA

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; BIOLOGICAL MARKER; CREATINE KINASE; MICRORNA; MICRORNA 1; MICRORNA 141; MICRORNA 192; MICRORNA 200A; MICRORNA 200B; MICRORNA 200C; MICRORNA 205; MICRORNA 21; MICRORNA 210; MICRORNA 29A; MICRORNA 29B; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P48; PROTEIN P53; RIBONUCLEASE; RNA INDUCED SILENCING COMPLEX;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ALZHEIMER DISEASE; APOPTOSIS; BLADDER CANCER; BREAST CANCER; CANCER DIAGNOSIS; CANCER PROGNOSIS; CELL COMMUNICATION; CHRONIC LYMPHATIC LEUKEMIA; COLON CANCER; CROHN DISEASE; DIAGNOSTIC VALUE; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DOWN REGULATION; DUCHENNE MUSCULAR DYSTROPHY; ENDOMETRIUM CANCER; ENZYME ACTIVITY; EXOSOME; GLIOBLASTOMA; GLOMERULUS FILTRATION RATE; HUMAN; INFLAMMATION; LIVER CELL CARCINOMA; LUNG NON SMALL CELL CANCER; LYMPHOMA; METABOLIC DISORDER; MOLECULARLY TARGETED THERAPY; PANCREAS CANCER; PATHOGENESIS; PATHOPHYSIOLOGY; PLASMA; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN RNA BINDING; REVIEW; RISK ASSESSMENT; RNA ANALYSIS; RNA SEQUENCE; SALIVA; SCHIZOPHRENIA; SENSITIVITY AND SPECIFICITY; SINGLE NUCLEOTIDE POLYMORPHISM; SJOEGREN SYNDROME; SOLID TUMOR; STOMACH CANCER; SYSTEMIC LUPUS ERYTHEMATOSUS; TESTIS CANCER; TONGUE CANCER; TUMOR MICROENVIRONMENT; ULCERATIVE COLITIS; UPREGULATION; URINE; UROGENITAL TRACT TUMOR;

AUTOIMMUNE DISEASES; CELL COMMUNICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INFLAMMATION; METABOLIC DISEASES; MICRORNAS; NEOPLASMS; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84869741959     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1647     Document Type: Review

References (200)

1. Setoyama T, Ling H, Natsugoe S and Calin GA: Non-coding RNAs for medical practice in oncology. Keio J Med 60: 106-113, 2011.
2. Carninci P, Kasukawa T, Katayama S, et al: The transcriptional landscape of the mammalian genome. Science 309: 1559-1563, 2005.
3. Kapranov P, Drenkow J, Cheng J, Long J, Helt G, Dike S and Gingeras TR: Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays. Genome Res 15: 987-997, 2005. (Pubitemid 40994219)
4. Mercer TR, Dinger ME and Mattick JS: Long non-coding RNAs: insights into functions. Nat Rev Genet 10: 155-159, 2009.
5. Taft RJ, Pang KC, Mercer TR, Dinger M and Mattick JS: Non- coding RNAs: regulators of disease. J Pathol 220: 126-139, 2010.
6. Gupta RA, Shah N, Wang KC, et al: Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076, 2010.
7. Friedman RC, Farh KK, Burge CB and Bartel DP: Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105, 2009.
8. Lee RC, Feinbaum RL and Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854, 1993. (Pubitemid 24014542)
9. Bartel DP and Chen CZ: Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 5: 396-400, 2004. (Pubitemid 38529411)
10. Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang XJ and Qi Y: A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21: 1190-1203, 2007.
11. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH and Kim VN: MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23: 4051-4060, 2004. (Pubitemid 39472426)
12. Borchert GM, Lanier W and Davidson BL: RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 13: 1097-1101, 2006. (Pubitemid 44885920)
13. Hu HY, Yan Z, Xu Y, et al: Sequence features associated with microRNA strand selection in humans and flies. BMC Genomics 10: 413, 2009.
14. Fabian MR, Sonenberg N and Filipowicz W: Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379, 2010.
15. Fiorucci G, Chiantore MV, Mangino G, Percario ZA, Affabris E and Romeo G: Cancer regulator microRNA: potential relevance in diagnosis, prognosis and treatment of cancer. Curr Med Chem 19: 461-474, 2012.
16. Zen K and Zhang CY: Circulating microRNAs: a novel class of biomarkers to diagnose and monitor human cancers. Med Res Rev 32: 326-348, 2012.
17. Weber JA, Baxter DH, Zhang S, et al: The microRNA spectrum in 12 body fluids. Clin Chem 56: 1733-1741, 2010.
18. Wang K, Zhang S, Weber J, Baxter D and Galas DJ: Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 38: 7248-7259, 2010.
19. Zubakov D, Boersma AW, Choi Y, van Kuijk PF, Wiemer EA and Kayser M: MicroRNA markers for forensic body fluid identification obtained from microarray screening and quantitative RT-PCR confirmation. Int J Legal Med 124: 217-226, 2010.
20. Hanson EK, Lubenow H and Ballantyne J: Identification of forensically relevant body fluids using a panel of differentially expressed microRNAs. Anal Biochem 387: 303-314, 2009.
21. Weickmann JL and Glitz DG: Human ribonucleases. Quantitation of pancreatic-like enzymes in serum, urine, and organ preparations. J Biol Chem 257: 8705-8710, 1982. (Pubitemid 12004191)
22. Gibbings DJ, Ciaudo C, Erhardt M and Voinnet O: Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11: 1143-1149, 2009.
23. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ and Lotvall JO: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659, 2007. (Pubitemid 47214727)
24. Iguchi H, Kosaka N and Ochiya T: Secretory microRNAs as a versatile communication tool. Commun Integr Biol 3: 478-481, 2010.
25. Camussi G, Deregibus MC, Bruno S, Cantaluppi V and Biancone L: Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 78: 838-848, 2010.
26. Muralidharan-Chari V, Clancy JW, Sedgwick A and D'Souza-Schorey C: Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123: 1603-1611, 2010.
27. Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK and Calin GA: MicroRNAs in body fluids - the mix of hormones and biomarkers. Nat Rev Clin Oncol 8: 467-477, 2011.
28. Etheridge A, Lee I, Hood L, Galas D and Wang K: Extracellular microRNA: a new source of biomarkers. Mutat Res 717: 85-90, 2011.
29. Skog J, Wurdinger T, van Rijn S, et al: Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476, 2008.
30. Hunter MP, Ismail N, Zhang X, et al: Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3: e3694, 2008.
31. Michael A, Bajracharya SD, Yuen PS, Zhou H, Star RA, Illei GG and Alevizos I: Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis 16: 34-38, 2010.
32. Dimov I, Velickovic L and Stefanovic V: Urinary exosomes. Sci World J 9: 1107-1118, 2009.
33. Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, Raposo G and Hivroz C: TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol 168: 3235-3241, 2002. (Pubitemid 34250383)
34. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ and Geuze HJ: B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183: 1161-1172, 1996. (Pubitemid 26113979)
35. Thery C, Regnault A, Garin J, et al: Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol 147: 599-610, 1999. (Pubitemid 29523465)
36. Mears R, Craven RA, Hanrahan S, et al: Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 4: 4019-4031, 2004. (Pubitemid 39657475)
37. O'Neill HC and Quah BJ: Exosomes secreted by bacterially infected macrophages are proinflammatory. Sci Signal 1: 8, 2008.
38. Taylor DD and Gercel-Taylor C: MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110: 13-21, 2008. (Pubitemid 351853251)
39. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W and Geuze HJ: Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113: 3365-3374, 2000.
40. Huber V, Filipazzi P, Iero M, Fais S and Rivoltini L: More insights into the immunosuppressive potential of tumor exosomes. J Transl Med 6: 63, 2008.
41. Xiang X, Poliakov A, Liu C, et al: Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 124: 2621-2633, 2009.
42. Vallhov H, Gutzeit C, Johansson SM, et al: Exosomes containing glycoprotein 350 released by EBV-transformed B cells selectively target B cells through CD21 and block EBV infection in vitro. J Immunol 186: 73-82, 2011.
43. Shen J, Todd NW, Zhang H, et al: Plasma microRNAs as potential biomarkers for non-small-cell lung cancer. Lab Invest 91: 579-587, 2011.
44. Mitchell PS, Parkin RK, Kroh EM, et al: Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105: 10513-10518, 2008.
45. Gilad S, Meiri E, Yogev Y, et al: Serum microRNAs are promising novel biomarkers. PLoS One 3: e3148, 2008.
46. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y and Ochiya T: Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285: 17442-17452, 2010.
47. Turchinovich A, Weiz L, Langheinz A and Burwinkel B: Characterization of extracellular circulating microRNA. Nucleic Acids Res 39: 7223-7233, 2011.
48. Chen X, Ba Y, Ma L, et al: Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18: 997-1006, 2008.
49. Li J, Smyth P, Flavin R, et al: Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalin-fixed paraffin-embedded (FFPE) cells and snap-frozen cells. BMC Biotechnol 7: 36, 2007.
50. Xie Y, Todd NW, Liu Z, Zhan M and Fang H: Altered miRNA expression in sputum for diagnosis of non-small cell lung cancer. Lung Cancer 67: 170-176, 2010.
51. Tsujiura M, Ichikawa D, Komatsu S, et al: Circulating microRNAs in plasma of patients with gastric cancers. Br J Cancer 102: 1174-1179, 2010.
52. Huang Z, Huang D, Ni S, Peng Z, Sheng W and Du X: Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int J Cancer 127: 118-126, 2010.
53. Xi Y, Nakajima G, Gavin E, et al: Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin-fixed paraffin-embedded samples. RNA 13: 1668-1674, 2007. (Pubitemid 47481675)
54. Schöler N, Langer C and Kuchenbauer F: Circulating microRNAs as biomarkers - true blood? Genome Med 3: 72, 2011.
55. Wang G, Tam LS, Li EK, et al: Serum and urinary free microRNA level in patients with systemic lupus erythematosus. Lupus 20: 493-500, 2011.
56. Shaoqing Y, Ruxin Z, Guojun L, Zhiqiang Y, Hua H, Shudong Y and Jie Z: Microarray analysis of differentially expressed microRNAs in allergic rhinitis. Am J Rhinol Allergy 25: 242-246, 2011.
57. Zahm AM, Thayu M, Hand NJ, Horner A, Leonard MB and Friedman JR: Circulating microRNA is a biomarker of pediatric Crohn disease. J Pediatr Gastroenterol Nutr 53: 26-33, 2011.
58. Wu F, Guo NJ, Tian H, et al: Peripheral blood microRNAs distinguish active ulcerative colitis and Crohn's disease. Inflamm Bowel Dis 17: 241-250, 2011.
59. Zampetaki A, Kiechl S, Drozdov I, et al: Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 107: 810-817, 2010.
60. Karolina DS, Armugam A, Tavintharan S, Wong MTK, Lim SC, Sum CF and Jeyase K: MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus. PLos One 6: e22839, 2011.
61. Cogswell JP, Ward J, Taylor IA, et al: Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J Alzheimers Dis 14: 27-41, 2008. (Pubitemid 352039013)
62. Geekiyanage H, Jicha GA, Nelson PT and Chan C: Blood serum miRNA: non-invasive biomarkers for Alzheimer's disease. Exp Neurol 235: 491-496, 2012.
63. Beveridge NJ and Cairns MJ: MicroRNA dysregulation in schizophrenia. Neurobiol Dis 46: 263-271, 2012.
64. Mizuno H, Nakamura A, Aoki Y, et al: Identification of muscle-specific microRNAs in serum of muscular dystrophy animal models: promising novel blood-based markers for muscular dystrophy. PLoS One 6: e18388, 2011.
65. Laterza OF, Lim L, Garrett-Engele PW, et al: Plasma microRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem 55: 1977-1983, 2009.
66. Xu J, Zhao J, Evan G, Xiao C, Cheng Y and Xiao J: Circulating microRNAs: novel biomarkers for cardiovascular diseases. J Mol Med (Berl) 90: 865-875, 2012.
67. Li H, Guo L, Wu Q, Lu J, Ge Q and Lu Z: A comprehensive survey of maternal plasma miRNAs expression profiles using high-throughput sequencing. Clin Chim Acta 413: 568-576, 2012.
68. Chim SS, Shing TK, Hung EC, et al: Detection and characterization of placental microRNAs in maternal plasma. Clin Chem 54: 482-490, 2008. (Pubitemid 351348154)
69. Gunel T, Zeybek YG, Akçakaya P, Kalelioǧlu I, Benian A, Ermis H and Aydinli K: Serum microRNA expression in pregnancies with preeclampsia. Genet Mol Res 10: 4034-4040, 2011.
70. Calin GA, Sevignani C, Dumitru CD, et al: Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101: 2999-3004, 2004. (Pubitemid 38327724)
71. Asaga S, Kuo C, Nguyen T, Terpenning M, Giuliano AE and Hoon DS: Direct serum assay for microRNA-21 concentrations in early and advanced breast cancer. Clin Chem 57: 84-91, 2011.
72. Cho WC: MicroRNAs in cancer-from research to therapy. Biochim Biophys Acta 1805: 209-217, 2010.
73. Cho WC: MicroRNAs: potential biomarkers for cancer diagnosis, prognosis and targets for therapy. Int J Biochem Cell Biol 42: 1273-1281, 2010.
74. Lu J, Getz G, Miska EA, et al: MicroRNA expression profiles classify human cancers. Nature 435: 834-838, 2005. (Pubitemid 40839735)
75. Chan JA, Krichevsky AM and Kosik KS: MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65: 6029-6033, 2005. (Pubitemid 40994386)
76. Iorio MV, Ferracin M, Liu CG, et al: MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070, 2005. (Pubitemid 41161233)
77. Markou A, Tsaroucha EG, Kaklamanis L, et al: Prognostic value of mature microRNA-21 and microRNA-205 overexpression in nonsmall cell lung cancer by quantitative real-time RT-PCR. Clin Chem 54: 1696-1704, 2008.
78. Schetter AJ, Leung SY, Sohn JJ, et al: MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 299: 425-436, 2008. (Pubitemid 351185951)
79. Huang YS, Dai Y, Yu XF, et al: Microarray analysis of microRNA expression in hepatocellular carcinoma and non-tumorous tissues without viral hepatitis. J Gastroenterol Hepatol 23: 87-94, 2008. (Pubitemid 350265207)
80. Ladeiro Y, Couchy G, Balabaud C, et al: MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 47: 1955-1963, 2008. (Pubitemid 351952843)
81. Bandrés E, Cubedo E, Agirre X, et al: Identification by real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer 5: 29, 2006.
82. Slaby O, Svoboda M, Fabian P, et al: Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncology 72: 397-402, 2007. (Pubitemid 351238155)
83. Motoyama K, Inoube H, Takatsuno Y, et al: Over- and under-expressed microRNAs in human colorectal cancer. Int J Oncol 34: 1069-1075, 2009.
84. Wang CJ, Zhou ZG, Wang L, et al: Clinicopathological significance of microRNA-31, -143 and -145 expression in colorectal cancer. Dis Markers 26: 27-34, 2009.
85. Yan LIX, Huang XF, Shao Q, et al: MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 14: 2348-2360, 2008.
86. Valastyan S, Reinhardt F, Benaich N, et al: A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137: 1032-1046, 2009.
87. Guo J, Miao Y, Xiao B, et al: Differential expression of microRNA species in human gastric cancer versus non-tumorous tissues. J Gastroenterol Hepatol 24: 652-657, 2009.
88. Veerla S, Lindgren D, Kvist A, et al: MiRNA expression in urothelial carcinomas: important roles of miR-10a, miR-222, miR-125b, miR-7 and miR-452 for tumor stage and metastasis, and frequent homozygous losses of miR-31. Int J Cancer 124: 2236-2242, 2009.
89. Rosenfeld N, Aharonov R, Meiri E, et al: MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 26: 462-469, 2008. (Pubitemid 351501813)
90. He JF, Luo YM, Wan XH and Jiang D: Biogenesis of miRNA-195 and its role in biogenesis, the cell cycle, and apoptosis. J Biochem Mol Toxicol 25: 404-408, 2011.
91. Donzelli S, Fontemaggi G, Fazi F, et al: MicroRNA-128-2 targets the transcriptional repressor E2F5 enhancing mutant p53 gain of function. Cell Death Differ 19: 1038-1048, 2012.
92. Yin R, Bao W, Xing Y, Xi T and Gou S: MiR-19b-1 inhibits angiogenesis by blocking cell cycle progression of endothelial cells. Biochem Biophys Res Commun 417: 771-776, 2012.
93. Enkelmann A, Heinzelmann J, von Eggeling F, et al: Specific protein and miRNA patterns characterise tumour-associated fibroblasts in bladder cancer. J Cancer Res Clin Oncol 137: 751-759, 2011.
94. Schaar DG, Medina DJ, Moore DF, Strair RK and Ting YI: miR-320 targets transferrin receptor 1 (CD71) and inhibits cell proliferation. Exp Hematol 37: 245-255, 2009.
95. Ichimi T, Enokida H, Okuno Y, et al: Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int J Cancer 125: 345-352, 2009.
96. Chiyomaru T, Enokida H, Tatarano S, et al: miR-145 and miR-133a function as tumour suppressors and directly regulate FSCN1 expression in bladder cancer. Br J Cancer 102: 883-891, 2010.
97. Ostenfeld MS, Bramsen JB, Lamy P, et al: miR-145 induces caspase-dependent and -independent cell death in urothelial cancer cell lines with targeting of an expression signature present in Ta bladder tumors. Oncogene 29: 1073-1084, 2010.
98. Aprelikova O, Yu X, Palla J, et al: The role of miR-31 and its target gene SATB2 in cancer-associated fibroblasts. Cell Cycle 9: 4387-4398, 2010.
99. Rana TM: Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol 8: 23-36, 2007.
100. Bullock MD, Sayan AE, Packham GK and Mirnezami AH: microRNAs: critical regulators of epithelial to mesenchymal (EMT) and mesenchymal to epithelial transition (MET) in cancer progression. Biol Cell 104: 3-12, 2012.
101. Avila-Moreno F, Urrea F and Ortiz-Quintero B: MicroRNAs in diagnosis and prognosis in lung cancer. Rev Invest Clin 63: 516-535, 2011.
102. Segura MF, Belitskaya-Lévy I, Rose AE, et al: Melanoma microRNA signature predicts post-recurrence survival. Clin Cancer Res 16: 1577-1586, 2010.
103. Yu SL, Chen HY, Chang GC, et al: MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cell 13: 48-57, 2008.
104. Zhou N and Mo YY: Roles of microRNAs in cancer stem cells. Front Biosci 4: 810-818, 2012.
105. Ho AS, Huang X, Cao H, et al: Circulating miR-210 as a novel hypoxia marker in pancreatic cancer. Transl Oncol 3: 109-113, 2010.
106. Resnick KE, Alder H, Hagan JP, et al: 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, 2009.
107. Ng EK, Chong WW, Jin H, et al: Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut 58: 1375-1381, 2009.
108. Wentz-Hunter KK and Potashkin JA: The role of miRNAs as key regulators in the neoplastic microenvironment. Mol Biol Int 2011: 839872, 2011.
109. Kosaka N, Iguchi H and Ochiya T: Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101: 2087-2092, 2010.
110. Roth C, Rack B, Muller V, Janni W, Pantel K and Schwarzenbach H: Circulating microRNAs as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res 12: R90, 2010.
111. Yu L, Todd NW, Xing L, Xie Y, Zhang H, Liu Z and Jiang F: Early detection of lung adenocarcinoma in sputum by a panel of microRNA markers. Int J Cancer 127: 2870-2878, 2010.
112. Xing L, Todd NW, Yu L, Fang H and Jiang F: Early detection of squamous cell lung cancer in sputum by a panel of microRNA markers. Mod Pathol 8: 1157-1164, 2010.
113. Pezzolesi MG, Platzer P, Waite KA and Eng C: Differential expression of PTEN-targeting microRNAs miR-19a and miR-21 in Cowden syndrome. Am J Hum Genet 82: 1141-1149, 2008. (Pubitemid 351615147)
114. Zhu S, Si ML, Wu H and Mo YY: MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem 282: 14328-14336, 2007. (Pubitemid 47100416)
115. Du Rieu MC, Torrisani J, Selves J, et al: MicroRNA-21 is induced early in pancreatic ductal adenocarcinoma precursor lesions. Clin Chem 56: 603-612, 2010.
116. Zhang HL, Yang LF, Zhu Y, et al: Serum miRNA-21: elevated levels in patients with metastatic hormone-refractory prostate cancer and potential predictive factor for the efficacy of docetaxel-based chemotherapy. Prostate 71: 326-331, 2011.
117. Shen J, Liu Z, Todd NW, et al: Diagnosis of lung cancer in individuals with solitary pulmonary nodules by plasma microRNA biomarkers. BMC Cancer 11: 374, 2011.
118. Wei J, Gao W, Zhu CJ, Liu YQ, Mei Z, Cheng T and Shu YQ: Identification of plasma micro-RNA-21 as a biomarker for early detection and chemosensitivity of non-small cell lung cancer. Chin J Cancer 30: 407-414, 2011.
119. Oh HK, Tan AL, Das K, et al: Genomic loss of miR-486 regulates tumor progression and the OLFM4 anti-apoptotic factor in gastric cancer. Clin Cancer Res 17: 2657-2667, 2011.
120. Mees ST, Mardin WA, Sielker S, et al: Involvement of CD40 targeting miR-224 and miR-486 on the progression of pancreatic ductal adenocarcinomas. Ann Surg Oncol 16: 2339-2350, 2009.
121. Bansal A, Lee IH, Hong X, et al: Feasibility of microRNAs as biomarkers for Barrett's esophagus progression: a pilot cross-sectional, phase 2 biomarker study. Am J Gastroenterol 106: 1055-1063, 2011.
122. Huang X, Ding L, Bennewith KL, et al: Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 35: 856-867, 2009.
123. Roth C, Kasimir-Bauer S, Pantel K and Schwarzenbach H: Screening for circulating nucleic acids and caspase activity in the peripheral blood as potential diagnostic tools in lung cancer. Mol Oncol 5: 281-291, 2011.
124. Zheng D, Haddadin S, Wang Y, Gu LQ, Perry MC, Freter CE and Wang MX: Plasma microRNAs as novel biomarkers for early detection of lung cancer. Int J Clin Exp Pathol 4: 575-586, 2011.
125. Heegaard NH, Schetter AJ, Welsh JA, Yoneda M, Bowman ED and Harris CC: Circulating microRNA expression profiles in early stage non-small cell lung cancer. Int J Cancer 130: 1378-1386, 2012.
126. Bianchi F, Nicassio F, Marzi M, et al: A serum circulating miRNA diagnostic test to identify asymptomatic high-risk individuals with early stage lung cancer. EMBO Mol Med 3: 495-503, 2011.
127. Bockmeyer CL, Christgen M, Müller M, et al: MicroRNA profiles of healthy basal and luminal mammary epithelial cells are distinct and reflected in different breast cancer subtypes. Breast Cancer Res Treat 130: 735-745, 2011.
128. Blenkiron C, Goldstein LD, Thorne NP, et al: MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol 8: 214, 2007.
129. Adams BD, Guttilla IK and White BA: Involvement of microRNAs in breast cancer. Semin Reprod Med 26: 522-536, 2008.
130. Enerly E, Steinfeld I, Kleivi K, et al: miRNA-mRNA integrated analysis reveals roles for miRNAs in primary breast tumors. PLoS One 6: e16915, 2011.
131. Yu F, Yao H, Zhu P, et al: let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131: 1109-1123, 2007. (Pubitemid 350235025)
132. Tavazoie SF, Alarcón C, Oskarsson T, et al: Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451: 147-152, 2008.
133. Hurteau GJ, Carlson JA, Spivack SD and Brock GJ: Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res 67: 7972-7976, 2007. (Pubitemid 47395127)
134. Bertos NR and Park M: Breast cancer - one term, many entities? J Clin Invest 121: 3789-3796, 2011.
135. Heneghan HM, Miller N and Kerin MJ: Circulating microRNAs: promising breast cancer. Breast Cancer Res 13: 402, 2011.
136. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A and Ratajczak MZ: Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20: 1487-1495, 2006. (Pubitemid 44264090)
137. Ohshima K, Inoue K, Fujiwara A, et al: Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One 5: e13247, 2010.
138. Gourzones C, Gelin A, Bombik I, et al: Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells. Virol J 7: 271, 2010.
139. Luo SS, Ishibashi O, Ishikawa G, et al: Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod 81: 717-729, 2009.
140. Yang M, Chen J, Su F, et al: Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10: 117, 2011.
141. Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH and Filipowicz W: Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med 15: 31-33, 2009.
142. Morita K, Taketomi A, Shirabe K, et al: Clinical significance and potential of hepatic microRNA-122 expression in hepatitis C. Liver Int 31: 474-484, 2011.
143. Wang K, Zhang S, Marzolf B, et al: Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA 106: 4402-4407, 2009.
144. Zhang Y, Jia Y, Zheng R, et al: Plasma microRNA-122 as a biomarker for viral-, alcohol-, and chemical-related hepatic diseases. Clin Chem 56: 1830-1838, 2010.
145. 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 50: 136-142, 2011.
146. Tomimaru Y, Eguchi H, Nagano H, et al: Circulating microRNA-21 as a novel biomarker for hepatocellular carcinoma. J Hepatol 56: 167-175, 2012.
147. Cermelli S, Ruggieri A, Marrero JA, Ioannou GN and Beretta L: Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS One 6: e23937, 2011.
148. Qi P, Cheng SQ, Wang H, Li N, Chen YF and Gao CF: Serum microRNAs as biomarkers for hepatocellular carcinoma in Chinese patients with chronic hepatitis B virus infection. PLoS One 6: e28486, 2011.
149. Ikeda Y, Tanji E, Makino N, Kawata S and Furukawa T: MicroRNAs associated with mitogen-activated protein kinase in human pancreatic cancer. Mol Cancer Res 10: 259-269, 2012.
150. Habbe N, Koorstra J, Mendell J, et al: MicroRNA miR-155 is a biomarker of early pancreatic neoplasia. Cancer Biol Ther 8: 340-346, 2009.
151. La Conti JL, Shivapurkar N, Preet A, et al: Tissue and serum microRNAs in the KrasG12D transgenic animal model and in patients with pancreatic cancer. PLoS One 6: e20687, 2011.
152. Morimura R, Komatsu S, Ichikawa D, et al: Novel diagnostic value of circulating miR-18a in plasma of patients with pancreatic cancer. Br J Cancer 105: 1733-1740, 2011.
153. Liu R, Chen X, Du Y, et al: Serum microRNA expression profile as a biomarker in the diagnosis and prognosis of pancreatic cancer. Clin Chem 58: 610-618, 2012.
154. Hwang JH, Voortman J, Giovannetti E, et al: Identification of microRNA-21 as a biomarker for chemoresistance and clinical outcome following adjuvant therapy in resectable pancreatic cancer. PLoS One 5: e10630, 2010.
155. Shigehara K, Yokomuro S, Ishibashi O, et al: Real-time PCR-based analysis of the human bile microRNAome identifies miR-9 as a potential diagnostic biomarker for biliary tract cancer. PLoS One 6: e23584, 2011.
156. Komatsu S, Ichikawa D, Takeshita H, et al: Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer 105: 104-111, 2011.
157. Chiang Y, Zhou X, Wang Z, et al: Expression levels of microRNA-192 and -215 in gastric carcinoma. Pathol Oncol Res 18: 585-591, 2012.
158. Wang J, Zhang J, Wu J, et al: MicroRNA-610 inhibits the migration and invasion of gastric cancer cells by suppressing the expression of vasodilator-stimulated phosphoprotein. Eur J Cancer [Epub ahead of print] 2011.
159. Liu H, Zhu L, Liu B, et al: Genome-wide microRNA profiles identify miR-378 as a serum biomarker for early detection of gastric cancer. Cancer Lett 316: 196-203, 2012.
160. Wu J, Wu G, Lv L, et al: MicroRNA-34a inhibits migration and invasion of colon cancer cells via targeting to Fra-1. Carcinogenesis 33: 519-528, 2012.
161. Nugent M, Miller N and Kerin MJ: MicroRNAs in colorectal cancer: function, dysregulation and potential as novel biomarkers. Eur J Surg Oncol 37: 649-654, 2011.
162. 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 6: e17745, 2011.
163. Wulfken LM, Moritz R, Ohlmann C, et al: MicroRNAs in renal cell carcinoma: diagnostic implications of serum miR-1233 levels. PLoS One 6: e25787, 2011.
164. Mahn R, Heukamp LC, Rogenhofer S, von Ruecker A, Müller SC and Ellinger J: Circulating microRNAs (miRNA) in serum of patients with prostate cancer. Urology 77: 9-16, 2011.
165. Lodes MJ, Caraballo M, Suciu D, Munro S, Kumar A and Anderson B: Detection of cancer with serum miRNAs on an oligonucleotide microarray. PLoS One 4: e6229, 2009.
166. Brase JC, Johannes M, Schlomm T, et al: Circulating miRNAs are correlated with tumor progression in prostate cancer. Int J Cancer 128: 608-616, 2010.
167. Moltzahn F, Olshen AB, Baehner L, et al: Microfluidic-based multiplex qRT-PCR identifies diagnostic and prognostic microRNA signatures in the sera of prostate cancer patients. Cancer Res 71: 550-560, 2011.
168. Wach S, Nolte E, Szczyrba J, et al: MicroRNA profiles of prostate carcinoma detected by multiplatform microRNA screening. Int J Cancer 130: 611-621, 2012.
169. Kuwabara Y, Ono K, Horie T, et al: Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate the existence of myocardial damage. Circ Cardiovasc Genet 4: 446-454, 2011.
170. 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 28: 655-661, 2010.
171. Selth LA, Townley S, Gillis JL, et al: Discovery of circulating microRNAs associated with human prostate cancer using a mouse model of disease. Int J Cancer 131: 652-661, 2012.
172. Gonzales JC, Fink LM, Goodman OB Jr, Symanowski JT, Vogelzang NJ and Ward DC: Comparison of circulating MicroRNA 141 to circulating tumor cells, lactate dehydrogenase, and prostate-specific antigen for determining treatment response in patients with metastatic prostate cancer. Clin Genitourin Cancer 9: 39-45, 2011.
173. Lin SC, Liu CJ, Lin JA, et al: miR-24 up-regulation in oral carcinoma: positive association from clinical and in vitro analysis. Oral Oncol 46: 204-208, 2010.
174. Park NJ, Zhou H, Elashoff D, Henson BS, Kastratovic DA, Abemayor E and Wong DT: Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin Cancer Res 15: 5473-5477, 2009.
175. 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 141: 672-675, 2008. (Pubitemid 351667616)
176. Cheng AM, Byrom MW, Shelton J and Ford LP: Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 33: 1290-1297, 2005. (Pubitemid 41439922)
177. Si ML, Zhu S, Wu H, Lu Z, Wu F and Mo YY: miR-21-mediated tumor growth.
178. Stamatopoulos B, Meuleman N, Haibe-Kains B, et al: MicroRNA-29c and microRNA-223 downregulation has in vivo significance in chronic lymphocytic leukemia and improves disease risk stratification. Blood 113: 5237-5245, 2009.
179. Moussay E, Wang K, Cho JH, et al: MicroRNA as biomarkers and regulators in B-cell chronic lymphocytic leukemia. Proc Natl Acad Sci USA 108: 6573-6578, 2011.
180. Fulci V, Chiaretti S, Goldoni M, et al: Quantitative technologies establish a novel microRNA profile of chronic lymphocytic leukemia. Blood 109: 4944-4951, 2007. (Pubitemid 46827793)
181. Huang J and Mo YY: Role of microRNAs in leukemia stem cells. Front Biosci (Schol Ed) 4: 799-809, 2012.
182. Zhu YD, Wang L, Sun C, et al: Distinctive microRNA signature is associated with the diagnosis and prognosis of acute leukemia. Med Oncol [Epub ahead of print] 2011.
183. 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 4: e5532, 2009.
184. Aqeilan RI, Calin GA and Croce CM: miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ 17: 215-220, 2010.
185. Cammarata G, Augugliaro L, Salemi D, et al: Differential expression of specific microRNA and their targets in acute myeloid leukemia. Am J Hematol 85: 331-339, 2010.
186. Tsang WP and Kwok TT: Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis 13: 1215-1222, 2008.
187. Calin GA, Dumitru CD, Shimizu M, et al: Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 99: 15524-15529, 2002. (Pubitemid 35403967)
188. Pons A, Nomdedeu B, Navarro A, et al: Hematopoiesis-related microRNA expression in myelodysplastic syndromes. Leuk Lymphoma 50: 1854-1859, 2009.
189. Zuo Z, Calin GA, De Paula HM, et al: Circulating microRNAs let-7a and miR-16 predict progression-free survival and overall survival in patients with myelodysplastic syndrome. Blood 118: 413-415, 2011.
190. Huang JJ, Yu J, Li JY, Liu YT and Zhong RQ: Circulating microRNA expression is associated with genetic subtype and survival of multiple myeloma. Med Oncol [Epub ahead of print] 2012.
191. Yu DC, Li QG, Ding LXW and Ding YT: Circulating microRNAs: potential biomarkers for cancer. Int J Mol Sci 12: 2055-2063, 2011.
192. Duttagupta R, Jiang R, Gollub J, Getts RC and Jones KE: Impact of cellular miRNAs on circulating miRNA biomarker signatures. PLoS One 6: e20769, 2011.
193. Pritchard CC, Kroh E, Wood B, et al: Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila) 5: 492-497, 2012.
194. McDonald JS, Milosevic D, Reddi HV, Grebe SK and Algeciras-Schimnich A: Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem 57: 833-840, 2011.
195. Reid G, Kirschner MB and van Zandwijk N: Circulating microRNAs: association with disease and potential use as biomarkers. Crit Rev Oncol Hematol 80: 193-208, 2011.
196. Wang Y, Zheng D, Tan Q, Wang MX and Gu LQ: Nanopore-based detection of circulating microRNAs in lung cancer patients. Nat Nanotechnol 6: 668-674, 2011.
197. Spiegel JC, Lorenzen JM and Thum T: Role of microRNAs in immunity and organ transplantation. Expert Rev Mol Med 13: e37, 2011.
198. Benner SA: Extracellular 'communicator RNA'. FEBS Lett 233: 225-228, 1988.
199. D'Alessandra Y, Pompilio G and Capogrossi MC: MicroRNAs and myocardial infarction. Curr Opin Cardiol 27: 228-235, 2012.
200. Ha TY: The role of microRNAs in regulatory T cells and in the immune response. Immune Netw 11: 11-41, 2011.