Diagnostic applications of cell-free and circulating tumor cell-associated miRNAs in cancer patients

Expert Review of Molecular Diagnostics

Volumn 11, Issue 3, 2011, Pages 259-275

  Mostert, Bianca ^a   Sieuwerts, Anieta M ^b   Martens, John W M ^b   Sleijfer, Stefan ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

Author keywords

circulating tumor cells; diagnosis; drug target; microRNA; miRNA; prognosis; response prediction

Indexed keywords

CYCLIN D2; CYCLIN E; GEMCITABINE; MICRORNA; RIBONUCLEASE III; RNA INDUCED SILENCING COMPLEX; RNA POLYMERASE II;

BILE DUCT CARCINOMA; BREAST CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER OF UNKNOWN PRIMARY SITE; CANCER PATIENT; CANCER TISSUE; CELL FREE SYSTEM; COLON CANCER; COLORECTAL CANCER; DRUG TARGETING; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SILENCING; HEAD AND NECK CANCER; HUMAN; HYPOXIA; LIVER CELL CARCINOMA; LUNG NON SMALL CELL CANCER; MOLECULAR BIOLOGY; OVARY CANCER; PANCREAS CANCER; PRIMARY TUMOR; PROGNOSIS; PROSTATE CANCER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RHABDOMYOSARCOMA; RNA ANALYSIS; RNA STABILITY; STOMACH CANCER; TREATMENT RESPONSE; TUMOR EMBOLISM;

GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MOLECULAR DIAGNOSTIC TECHNIQUES; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; RNA INTERFERENCE;

EID: 79953821255     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/erm.11.11     Document Type: Review

References (91)

1. Cristofanilli M, Budd Gt, Ellis Mj et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 351(8), 781-791 (2004). Pivotal clinical study establishing the prognostic significance of circulating tumor cell (CTC) enumeration in metastasis breast cancer.
2. Cristofanilli M, Hayes DF, Budd GT et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J. Clin. Oncol. 23(7), 1420-1430 (2005).
3. Cohen SJ, Punt CJ, Iannotti N et al. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J. Clin. Oncol. 26(19), 3213-3221 (2008).
4. De Bono JS, Scher HI, Montgomery RB et al. Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin. Cancer Res. 14(19), 6302-6309 (2008).
5. Hayes DF, Cristofanilli M, Budd GT et al. Circulating tumor cells at each follow-up time point during therapy of metastatic breast cancer patients predict progression-free and overall survival. Clin. Cancer Res. 12(14 Pt 1), 4218-4224 (2006).
6. Attard G, Swennenhuis JF, Olmos D et al. Characterization of ERG, AR and PTEN gene status in circulating tumor cells from patients with castration-resistant prostate cancer. Cancer Res. 69(7), 2912-2918 (2009).
7. Leversha Ma, Han J, Asgari Z et al. Fluorescence in situ hybridization analysis of circulating tumor cells in metastatic prostate cancer. Clin. Cancer Res. 15(6), 2091-2097 (2009).
8. Pestrin M, Bessi S, Galardi F et al. Correlation of HER2 status between primary tumors and corresponding circulating tumor cells in advanced breast cancer patients. Breast Cancer Res. Treat. 118(3), 523-530 (2009).
9. Jiang Y, Palma JF, Agus DB, Wang Y, Gross ME. Detection of androgen receptor mutations in circulating tumor cells in castration-resistant prostate cancer. Clin. Chem. 56(9), 1492-1495 (2010).
10. Maheswaran S, Sequist LV, Nagrath S et al. Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med. 359(4), 366-377 (2008).
11. Munzone E, Nolé F, Zorzino L et al. Acquisition of HER2/neu over-expression on circulating tumor cells (CTCs) in patients (pts) with advanced breast cancer (ABC) during chemotherapy. J. Clin. Oncol. 26(15 Suppl.) (2008) (Abstract 11017).
12. Sieuwerts Am, Kraan J, Bolt-De Vries J et al. Molecular characterization of circulating tumor cells in large quantities of contaminating leukocytes by a multiplex real-time PCR. Breast Cancer Res. Treat. 118(3), 455-468 (2009).
13. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S. Stem cell and epithelial-mesenchymal transition markers are frequently over-expressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res. 11(4), R46 (2009).
14. Fehm T, Muller V, Aktas B et al. HER2 status of circulating tumor cells in patients with metastatic breast cancer: a prospective, multicenter trial. Breast Cancer Res. Treat. 124(2), 403-412 (2010).
15. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5), 843-854 (1993).
16. Mattick JS, Makunin IV. Non-coding RNA. Hum. Mol. Genet. 15(1), R17-R29 (2006).
17. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat. Rev. Cancer 6(11), 857-866 (2006). Comprehensive review on the use of miRNA profiling signatures in human cancers.
18. Wiemer EA. The role of microRNAs in cancer: no small matter. Eur. J. Cancer 43(10), 1529-1544 (2007).
19. 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(10), 997-1006 (2008).
20. Gilad S, Meiri E, Yogev Y et al. Serum microRNAs are promising novel biomarkers. PLoS ONE 3(9), e3148 (2008).
21. Mitchell PS, Parkin RK, Kroh EM et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl Acad. Sci. USA 105(30), 10513-10518 (2008). Pioneer study that established the feasibility of measurement of circulating miRNAs in serum or plasma.
22. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110(1), 13-21 (2008).
23. 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. 57(1), 84-91 (2011).
24. Brase JC, Wuttig D, Kuner R, Sultmann H. Serum microRNAs as non-invasive biomarkers for cancer. Mol. Cancer 9(1), 306 (2010).
25. 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).
26. Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 6(5), 376-385 (2005).
27. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science 318(5858), 1931-1934 (2007).
28. Miranda KC, Huynh T, Tay Y et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126(6), 1203-1217 (2006). Important study elucidating the far-stretched effects of miRNAs on gene expression.
29. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281-297 (2004).
30. Lu J, Getz G, Miska EA et al. MicroRNA expression profiles classify human cancers. Nature 435(7043), 834-838 (2005).
31. Rosenfeld N, Aharonov R, Meiri E et al. MicroRNAs accurately identify cancer tissue origin. Nat. Biotechnol. 26(4), 462-469 (2008).
32. Rosenwald S, Gilad S, Benjamin S et al. Validation of a microRNA-based qRT-PCR test for accurate identification of tumor tissue origin. Mod. Pathol. 23(6), 814-823 (2010).
33. Sempere LF, Christensen M, Silahtaroglu A et al. Altered microRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res. 67(24), 11612-11620 (2007).
34. Ferracin M, Veronese A, Negrini M. Micromarkers: miRNAs in cancer diagnosis and prognosis. Expert Rev. Mol. Diagn. 10(3), 297-308 (2010). Well-written and comprehensive review on the prognostic significance of miRNAs in cancer.
35. Yang H, Kong W, He L et al. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 68(2), 425-433 (2008).
36. Weiss GJ, Bemis LT, Nakajima E et al. EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines. Ann. Oncol. 19(6), 1053-1059 (2008).
37. Ji J, Shi J, Budhu A et al. MicroRNA expression, survival, and response to interferon in liver cancer. N. Engl. J. Med. 361(15), 1437-1447 (2009).
38. Salter KH, Acharya CR, Walters KS et al. An integrated approach to the prediction of chemotherapeutic response in patients with breast cancer. PLoS ONE 3(4), e1908 (2008).
39. Blower PE, Chung JH, Verducci JS et al. MicroRNAs modulate the chemosensitivity of tumor cells. Mol. Cancer Ther. 7(1), 1-9 (2008).
40. Rodriguez-Gonzalez FG, Sieuwerts AM, Smid M et al. MicroRNA-30c expression level is an independent predictor of clinical benefit of endocrine therapy in advanced estrogen receptor positive breast cancer. Breast Cancer Res. Treat. DOI: 10.1007/s10549-010-0940-x (2010) (Epub ahead of print).
41. Si Ml, Zhu S, Wu H, Lu Z, Wu F, Mo YY. miR-21-mediated tumor growth. Oncogene 26(19), 2799-2803 (2007).
42. Meng F, Henson R, Lang M et al. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology 130(7), 2113-2129 (2006).
43. Iorio MV, Casalini P, Piovan C et al. microRNA-205 regulates HER3 in human breast cancer. Cancer Res. 69(6), 2195-2200 (2009).
44. Kota J, Chivukula RR, O'donnell KA et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137(6), 1005-1017 (2009).
45. Krutzfeldt J, Rajewsky N, Braich R et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 438(7068), 685-689 (2005). Important study showing the feasibility of the use of miRNAs as drug targets.
46. Fabbri M, Croce CM, Calin GA. MicroRNAs in the ontogeny of leukemias and lymphomas. Leuk. Lymphoma 50(2), 160-170 (2009).
47. Lodes MJ, Caraballo M, Suciu D, Munro S, Kumar A, Anderson B. Detection of cancer with serum miRNAs on an oligonucleotide microarray. PLoS ONE 4(7), e6229 (2009).
48. Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Newell J, Kerin MJ. Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann. Surg. 251(3), 499-505 (2010).
49. Zhao H, Shen J, Medico L, Wang D, Ambrosone CB, Liu S. A pilot study of circulating miRNAs as potential biomarkers of early stage breast cancer. PLoS ONE 5(10), e13735 (2010).
50. Roth C, Rack B, Muller V, Janni W, Pantel K, Schwarzenbach H. Circulating microRNAs as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res. 12(6), R90 (2010).
51. Zhu W, Qin W, Atasoy U, Sauter ER. Circulating microRNAs in breast cancer and healthy subjects. BMC Res. Notes 2, 89 (2009).
52. 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. 28(10), 1721-1726 (2010).
53. Silva J, Garcia V, Zaballos A et al. Vesicle-related microRNAs in plasma of NSCLC patients and correlation with survival. Eur. Respir. J. 37(3), 617-623 (2011).
54. Brase JC, Johannes M, Schlomm T et al. Circulating miRNAs are correlated with tumor progression in prostate cancer. Int. J. Cancer 128(3), 608-616 (2011).
55. Moltzahn F, Olshen AB, Baehner L et al. Microfluidic based multiplex qRT-PCR identifies diagnostic and prognostic microRNA signatures in sera of prostate cancer patients. Cancer Res. 71(2), 550-560 (2011).
56. 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. 112(1), 55-59 (2009).
57. Van Niel G, Porto-Carreiro I, Simoes S, Raposo G. Exosomes: a common pathway for a specialized function. J. Biochem. 140(1), 13-21 (2006).
58. Tsujiura M, Ichikawa D, Komatsu S et al. Circulating microRNAs in plasma of patients with gastric cancers. Br. J. Cancer 102(7), 1174-1179 (2010).
59. Zhou H, Guo JM, Lou YR et al. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using microRNA as a marker. J. Mol. Med. 88(7), 709-717 (2010).
60. 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. 120(5), 183-193 (2011).
61. Yamamoto Y, Kosaka N, Tanaka M et al. MicroRNA-500 as a potential diagnostic marker for hepatocellular carcinoma. Biomarkers 14(7), 529-538 (2009).
62. 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 127(1), 118-126 (2010).
63. 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(10), 1375-1381 (2009).
64. Pu XX, Huang GL, Guo HQ et al. Circulating miR-221 directly amplified from plasma is a potential diagnostic and prognostic marker of colorectal cancer and is correlated with p53 expression. J. Gastroenterol. Hepatol. 25(10), 1674-1680 (2010).
65. Li A, Omura N, Hong SM 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. 70(13), 5226-5237 (2010).
66. Ho AS, Huang X, Cao H et al. Circulating miR-210 as a novel hypoxia marker in pancreatic cancer. Transl. Oncol. 3(2), 109-113 (2010).
67. 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. 14(9), 2588-2592 (2008).
68. Zhang C, Wang C, Chen X et al. Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin. Chem. 56(12), 1871-1879 (2010).
69. Chen JF, Mandel EM, Thomson JM et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38(2), 228-233 (2006).
70. 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. 400(1), 89-93 (2010).
71. Pigati L, Yaddanapudi SC, Iyengar R et al. Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS ONE 5(10), e13515 (2010).
72. Ji X, Takahashi R, Hiura Y, Hirokawa G, Fukushima Y, Iwai N. Plasma miR-208 as a biomarker of myocardial injury. Clin. Chem. 55(11), 1944-1949 (2009).
73. El-Hefnawy T, Raja S, Kelly L et al. Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics. Clin. Chem. 50(3), 564-573 (2004).
74. Katoh T, Sakaguchi Y, Miyauchi K et al. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 23(4), 433-438 (2009).
75. Zen K, Zhang CY. Circulating microRNAs: a novel class of biomarkers to diagnose and monitor human cancers. Med. Res. Rev. DOI: 10.1002/med.20215 (2010) (Epub ahead of print).
76. 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. 285(23), 17442-17452 (2010).
77. 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(12), 1470-1476 (2008).
78. Mostert B, Sleijfer S, Foekens JA, Gratama JW. Circulating tumor cells (CTCs): detection methods and their clinical relevance in breast cancer. Cancer Treat. Rev. 35(5), 463-474 (2009).
79. Breton F, Bennetau B, Lidereau R et al. A mesofluidic multiplex immunosensor for detection of circulating cytokeratin-positive cells in the blood of breast cancer patients. Biomed. Microdevices 13(1), 1-9 (2011).
80. Allard WJ, Matera J, Miller MC et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin. Cancer Res. 10(20), 6897-6904 (2004).
81. Lin Z, Wang X, Fewell C, Cameron J, Yin Q, Flemington EK. Differential expression of the miR-200 family microRNAs in epithelial and B cells and regulation of Epstein - Barr virus reactivation by the miR-200 family member miR-429. J. Virol. 84(15), 7892-7897 (2010).
82. Mestdagh P, Van Vlierberghe P, De Weer A et al. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 10(6), R64 (2009).
83. Sieuwerts Am, Kraan J, Bolt J et al. Anti-epithelial cell adhesion molecule antibodies and the detection of circulating normal-like breast tumor cells. J. Natl Cancer Inst. 101(1), 61-66 (2009).
84. Mostert B, Kraan J, Bolt-De Vries J et al. Detection of circulating tumor cells in breast cancer may improve through enrichment with anti-CD146. Breast Cancer Res. Treat. DOI: 10.1007/ s10549-010-0879-y (2010) (Epub ahead of print).
85. Gascoyne PR, Noshari J, Anderson TJ, Becker FF. Isolation of rare cells from cell mixtures by dielectrophoresis. Electrophoresis 30(8), 1388-1398 (2009).
86. Crosby ME, Kulshreshtha R, Ivan M, Glazer PM. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res. 69(3), 1221-1229 (2009).
87. Foekens JA, Sieuwerts AM, Smid M et al. Four miRNAs associated with aggressiveness of lymph node-negative, estrogen receptor-positive human breast cancer. Proc. Natl Acad. Sci. USA 105(35), 13021-13026 (2008).
88. Fasanaro P, Greco S, Lorenzi M et al. An integrated approach for experimental target identification of hypoxia-induced miR-210. J. Biol. Chem. 284(50), 35134-35143 (2009).
89. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5(7), 522-531 (2004).
90. Origene www.marligen.com
91. AllPrep DNA/RNA/Protein Mini Kit for simultaneous purification of DNA, RNA, and protein from cells and tissues www.qiagen.com