Circulating Tumor Cells in Hepatocellular Carcinoma: Detection Techniques, Clinical Implications, and Future Perspectives

Llovet, 2003, Hepatocellular carcinoma, Lancet, 362, 1907, 10.1016/S0140-6736(03)14964-1 Shariff, 2009, Hepatocellular carcinoma: current trends in worldwide epidemiology, risk factors, diagnosis and therapeutics, Expert Rev Gastroenterol Hepatol, 3, 353, 10.1586/egh.09.35 Mazzaferro, 2009, Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis, Lancet Oncol, 10, 35, 10.1016/S1470-2045(08)70284-5 Scatton, 2006, Fate and characterization of circulating tumor cells in a NOD/SCID mouse model of human hepatocellular carcinoma, Oncogene, 25, 4067, 10.1038/sj.onc.1209430 Pantel, 2010, Circulating tumour cells in cancer patients: challenges and perspectives, Trends Mol Med, 16, 398, 10.1016/j.molmed.2010.07.001 Jacob, 2007, Circulating tumor cellsdetection, molecular profiling and future prospects, Expert Rev Proteomics, 4, 741, 10.1586/14789450.4.6.741 Attard, 2011, Utilizing circulating tumor cells: challenges and pitfalls, Curr Opin Genet Dev, 21, 50, 10.1016/j.gde.2010.10.010 Gertler, 2003, Detection of circulating tumor cells in blood using an optimized density gradient centrifugation, Recent Results Cancer Res, 162, 149, 10.1007/978-3-642-59349-9_13 Vona, 2000, Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of, circulatingtumor cells, 156, 57 Lin, 2010, Portable filter-based microdevice for detection and characterization of circulating tumor cells, Clin Cancer Res, 16, 5011, 10.1158/1078-0432.CCR-10-1105 Xu, 2010, A cancer detection platform which measures telomerase activity from live circulating tumor cells captured on a microfilter, Cancer Res, 70, 6420, 10.1158/0008-5472.CAN-10-0686 Zheng, 2011, 3D microfilter device for viable circulating tumor cell (CTC) enrichment from blood, Biomed Microdevices, 13, 203, 10.1007/s10544-010-9485-3 McNiece, 1997, Large-scale isolation of CD34+ cells using the Amgen cell selection device results in high levels of purity and recovery, J Hematother, 6, 5, 10.1089/scd.1.1997.6.5 Neurauter, 2007, Cell isolation and expansion using Dynabeads, Adv Biochem Eng Biotechnol, 106, 41 Naume B, Borgen E, Tøssvik S, et al. Detection of isolated tumor cells in peripheral blood and in BM: evaluation of a new enrichment method. 2004;6:244–52. Talasaz, 2009, Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device, Proc Natl Acad Sci USA, 106, 3970, 10.1073/pnas.0813188106 Andreopoulou, 2012, Comparison of assay methods for detection of circulating tumor cells (CTCs) in metastatic breast cancer (MBC): AdnaGen AdnaTest BreastCancer Select/Detect versus Veridex CellSearch system, Int J Cancer, 130, 1590, 10.1002/ijc.26111 Miller, 2010, Significance of circulating tumor cells detected by the CellSearch system in patients with metastatic breast colorectal and prostate cancer, J Oncol, 2010, 10.1155/2010/617421 Radisky, 2008, Epithelial-mesenchymal transition and the stem cell phenotype, Cell Stem Cell, 2, 511, 10.1016/j.stem.2008.05.007 Nagrath, 2007, Isolation of rare circulating tumour cells in cancer patients by microchip technology, Nature, 450, 1235, 10.1038/nature06385 Stott, 2010, Isolation of circulating tumor cells using a microvortex-generating herringbone-chip, Proc Natl Acad Sci USA, 107, 18392, 10.1073/pnas.1012539107 Adams, 2008, Highly efficient circulating tumor cell isolation from whole blood and label-free enumeration using polymer-based microfluidics with an integrated conductivity sensor, J Am Chem Soc, 130, 8633, 10.1021/ja8015022 Zheng, 2011, A high-performance microsystem for isolating circulating tumor cells, Lab Chip, 11, 3269, 10.1039/c1lc20331b Saliba, 2010, Microfluidic sorting and multimodal typing of cancer cells in self-assembled magnetic arrays, Proc Natl Acad Sci USA, 107, 14524, 10.1073/pnas.1001515107 Hoshino, 2011, Microchip-based immunomagnetic detection of circulating tumor cells, Lab Chip, 11, 3449, 10.1039/c1lc20270g Wang, 2011, Nano “fly paper” technology for the capture of circulating tumor cells, Methods Mol Biol, 726, 141, 10.1007/978-1-61779-052-2_10 Mikolajczyk, 2011, Detection of EpCAM-Negative and cytokeratin-negative circulating tumor cells in peripheral blood, J Oncol, 2011, 252361, 10.1155/2011/252361 Tan, 2010, Versatile label free biochip for the detection of circulating tumor cells from peripheral blood in cancer patients, Biosens Bioelectron, 26, 1701, 10.1016/j.bios.2010.07.054 Bhagat, 2011, Pinched flow coupled shear-modulateed inertial microfluidics for high-throughputrare bloodcell separation, Lab Chip, 11, 1870, 10.1039/c0lc00633e Hur, 2011, Deformability-based cell classification and enrichment using inertial microfluidics, Lab Chip, 11, 912, 10.1039/c0lc00595a Gascoyne, 2009, Isolation of rare cells from cell mixtures by dielectrophoresis, Electrophoresis, 30, 1, 10.1002/elps.200800373 Moon, 2011, Continuous separation of breast cancer cells from blood samples using multi-orifice flow fractionation (MOFF) and dielectrophoresis (DEP), Lab Chip, 11, 1118, 10.1039/c0lc00345j Paterlini-Bréchot, 2000, Circulating tumorous cells in patients with hepatocellular carcinoma, Semin Cancer Biol, 10, 241, 10.1006/scbi.2000.0323 Ring AE, Zabaglo L, Ormerod MG, et al. Detection of circulating epithelial cells in the blood of patients with breast cancer: comparison of three techniques. 2005;92:906–12. Takao M, Takeda K. Enumeration, characterization, and collection of intact circulating tumor cells by cross contamination-free flow cytometry. 2011;79:107–17. Muthu, 2011, Targeted nanomedicine for detection and treatment of circulating tumor cells, Nanomedicine, 6, 579, 10.2217/nnm.11.17 He W, Wang H, Hartmann LC, et al. In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry. 2007;104:11760–5. Galanzha, 2009, In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser, Cancer Res, 69, 7926, 10.1158/0008-5472.CAN-08-4900 Galanzha, 2009, In vivo fiber-based multicolor photoacoustic detection and photothermal purging of metastasis in sentinel lymph nodes targeted by nanoparticles, J Biophoton, 2, 528, 10.1002/jbio.200910046 Nedosekin DA, Sarimollaoglu M, Ye JH, et al. In vivo ultra-fast photoacoustic flow cytometry of circulating human melanoma cells using near-infrared high-pulse rate lasers. 2011;79:825–33. Hsieh, 2006, High speed detection of circulating tumor cells, Biosens Bioelectron, 21, 1893, 10.1016/j.bios.2005.12.024 Scholtens, 2011, CellTracks TDI: an image cytometer for cell characterization, Cytometry A, 79, 203, 10.1002/cyto.a.21024 Henriksen M, Miller B, Newmark J, et al. Laser scanning cytometry and its applications: a pioneering technology in the field of quantitative imaging cytometry. 2011;102:161–205. Deng, 2008, Enrichment with anti-cytokeratin alone or combined with anti-EpCAM antibodies significantly increases the sensitivity for circulating tumor cell detection in metastatic breast cancer patients, Breast Cancer Res, 10, R69, 10.1186/bcr2131 Alix-Panabières, 2005, Detection of circulating prostate-specific antigen-secreting cells in prostate cancer patients, Clin Chem, 51, 1538, 10.1373/clinchem.2005.049445 Lu, 2010, Isolation of circulating epithelial and tumor progenitor cells with an invasive phenotype from breast cancer patients, Int J Cancer, 126, 669, 10.1002/ijc.24814 Kyo, 2008, Understanding and exploiting hTERT promoter regulation for diagnosis and treatment of human cancers, Cancer Sci, 99, 1528, 10.1111/j.1349-7006.2008.00878.x Waguri, 2003, Sensitive and specific detection of circulating cancer cells in patients with hepatocellular carcinoma; detection of human telomerase reverse transcriptase messenger RNA after immunomagnetic separation, Clin Cancer Res, 9, 3004 Min, 2009, High expression of Snail mRNA in blood from hepatocellular carcinoma patients with extra-hepatic metastasis, Clin Exp Metastasis, 26, 759, 10.1007/s10585-009-9275-6 Zhang, 2011, Lens culinaris agglutinin-reactive fraction of alpha-fetoprotein as a marker of prognosis and a monitor of recurrence of hepatocellular carcinoma after curative liver resection, Ann Surg Oncol, 18, 2218, 10.1245/s10434-011-1613-7 Yang, 2008, Significance of CD90+ cancer stem cells in human liver cancer, Cancer Cell, 13, 153, 10.1016/j.ccr.2008.01.013 Yang, 2008, Identification of local and circulating cancer stem cells in human liver cancer, Hepatology, 47, 919, 10.1002/hep.22082 Fan, 2011, Prediction of posthepatectomy recurrence of hepatocellular carcinoma by circulating cancer stem cells: a prospective study, Ann Surg, 254, 569, 10.1097/SLA.0b013e3182300a1d Collins, 2005, Prospective identification of tumorigenic prostate cancer stem cells, Cancer Res, 65, 10946, 10.1158/0008-5472.CAN-05-2018 Liu, 2006, Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma, Mol Cancer, 5, 67, 10.1186/1476-4598-5-67 de Boer, 1999, Expression of Ep-CAM in normal, regenerating, metaplastic, and neoplastic liver, J Pathol, 188, 201, 10.1002/(SICI)1096-9896(199906)188:2<201::AID-PATH339>3.0.CO;2-8 Schmelzer, 2006, The phenotypes of pluripotent human hepatic progenitors, Stem Cells, 24, 1852, 10.1634/stemcells.2006-0036 Proca, 2000, MOC31 immunoreactivity in proimary and metastatic carcinoma of the liver, Appl Immunohistochem Mol Morphol, 8, 120, 10.1097/00129039-200006000-00006 Porcell, 2000, Immunohistochemical analysis of hepatocellular and adenocarcinoma in the liver: mOC31 compares favorably with other putative markers, Mod Pathol, 13, 773, 10.1038/modpathol.3880134 Went, 2004, Frequent EpCam protein expression in human carcinomas, Hum Pathol, 35, 122, 10.1016/j.humpath.2003.08.026 Xu, 2011, Isolation of circulating tumor cells in patients with hepatocellular carcinoma using a novel cell separation strategy, Clin Cancer Res, 17, 3783, 10.1158/1078-0432.CCR-10-0498 Ashwell, 1982, Carbohydrate-specific receptors of the liver, Annu Rev Biochem, 51, 531, 10.1146/annurev.bi.51.070182.002531 Spiess, 1990, The asialoglycoprotein receptor: a model for endocytic transport receptors, Biochemistry, 29, 10009, 10.1021/bi00495a001 Wong, 1999, Hematogenous dissemination of hepatocytes and tumor cells after surgical resection of hepatocellular carcinoma: a quantitative analysis, Clin Cancer Res, 5, 4021 Zhou, 2008, Edmondson-Steiner grading increases the predictive efficiency of TNM staging for longterm survival of patients with hepatocellular carcinoma after curative resection, World J Surg, 32, 1748, 10.1007/s00268-008-9615-8 Polakis, 1999, The oncogenic activation of beta-catenin, Curr Opin Genet Dev, 9, 15, 10.1016/S0959-437X(99)80003-3 Bressac, 1991, Selective G to T mutations of p53 gene in hepatocellular carcinoma from southern Africa, Nature, 350, 429, 10.1038/350429a0 Ross, 2003, The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy, Oncologist, 8, 307, 10.1634/theoncologist.8-4-307 Bacaksiz, 2008, Determination of HER-2/Neu status in hepatocellular carcinoma cases, Genet Test, 12, 211, 10.1089/gte.2007.0095 Liu, 2009, Increased expression of ErbB-2 in liver is associated with hepatitis B x antigen and shorter survival in patients with liver cancer, Int J Cancer, 125, 1894, 10.1002/ijc.24580 Shackleton, 2009, Heterogeneity in cancer: cancer stem cells versus clonal evolution, Cell, 138, 822, 10.1016/j.cell.2009.08.017 Hermann, 2008, Metastatic cancer stem cells: a new target for anti-cancer therapy?, Cell Cycle, 7, 188, 10.4161/cc.7.2.5326 Mikhail, 2011, Liver cancer stem cells, Int J Hepatol, 2011, 486954, 10.4061/2011/486954 Bonnomet, 2010, Epithelial-to-mesenchymal transitions and circulating tumor cells, J Mammary Gland Biol Neoplasia, 15, 261, 10.1007/s10911-010-9174-0 Ma, 2007, Identification and characterization of tumorigenic liver cancer stem/progenitor cells, Gastroenterology, 132, 2542, 10.1053/j.gastro.2007.04.025 Yamashita, 2009, EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features, Gastroenterology, 136, 1012, 10.1053/j.gastro.2008.12.004 Haraguchi, 2010, CD13 is a therapeutic target in human liver cancer stem cells, J Clin Invest, 120, 3326, 10.1172/JCI42550 Chiba, 2006, Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties, Hepatology, 44, 240, 10.1002/hep.21227 Shi, 2008, Identification of side population cells in human hepatocellular carcinoma cell lines with stepwise metastatic potentials, J Cancer Res Clin Oncol, 134, 1155, 10.1007/s00432-008-0407-1 Cao, 2011, Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines, BMC Gastroenterol, 11, 71, 10.1186/1471-230X-11-71 Uchida, 2010, Analogy between sphere forming ability and stemness of human hepatoma cells, Oncol Rep, 24, 1147 Hiraiwa, 2008, Clinical significance of circulating tumor cells in blood from patients with gastrointestinal cancers, Ann Surg Oncol, 15, 3092, 10.1245/s10434-008-0122-9 Tanaka, 2010, CEA-antigen and SCC-antigen mRNA expression in peripheral blood predict hematogenous recurrence after resection in patients with esophageal cancer, Ann Surg Oncol, 17, 2779, 10.1245/s10434-010-1075-3 Peach, 2010, Prognostic significance of circulating tumour cells following surgical resection of colorectal cancers: a systematic review, Br J Cancer, 102, 1327, 10.1038/sj.bjc.6605651 Salnikov, 2009, Cancer stem cell marker expression in hepatocellular carcinoma and liver metastases is not sufficient as single prognostic parameter, Cancer Lett, 275, 185, 10.1016/j.canlet.2008.10.015 Toso, 2011, Liver transplantation for hepatocellular carcinoma: five steps to prevent recurrence, Am J Transplant, 11, 2031, 10.1111/j.1600-6143.2011.03689.x Wicha, 2011, Circulating tumor cells: not all detected cells are bad and not all bad cells aredetected, J Clin Oncol, 29, 1508, 10.1200/JCO.2010.34.0026 Baeuerle, 2007, EpCAM (CD326) finding its role in cancer, Br J Cancer, 96, 417, 10.1038/sj.bjc.6603494 Colombo, 2011, Evidence of distinct tumour-propagating cell populations with different properties in primary human hepatocellular carcinoma, PLoS One, 6, e21369, 10.1371/journal.pone.0021369 Raimondi, 2011, Epithelial-mesenchymal transition and stemness features in circulating tumorcells from breast cancer patients, Breast Cancer Res Treat, 130, 449, 10.1007/s10549-011-1373-x Navin, 2011, Future medical applications of single-cell sequencing in cancer, Genome Med, 3, 31, 10.1186/gm247 Liu, 2011, The power and the promise of liver cancer stem cell markers, Stem Cells Dev, 20, 2023, 10.1089/scd.2011.0012