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Cancer Cell International
Published in: Cancer Cell International 1/2019

Open Access 01-12-2019 | Metastasis | Review

Circulating tumor cells in precision oncology: clinical applications in liquid biopsy and 3D organoid model

Authors: Chang Yang, Bai-Rong Xia, Wei-Lin Jin, Ge Lou

Published in: Cancer Cell International | Issue 1/2019

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Abstract

Circulating tumor cells (CTCs) are a rare subset of cells found in the blood of patients with solid tumors, which function as a seed for metastases. Cancer cells metastasize through the bloodstream either as single migratory CTCs or as multicellular groupings—CTC clusters. The CTCs preserve primary tumor heterogeneity and mimic tumor properties, and may be considered as clinical biomarker, preclinical model, and therapeutic target. The potential clinical application of CTCs is being a component of liquid biopsy. CTCs are also good candidates for generating preclinical models, especially 3D organoid cultures, which could be applied in drug screening, disease modeling, genome editing, tumor immunity, and organoid biobanks. In this review, we summarize current knowledge on the value and promise of evolving CTC technologies and highlight cutting-edge research on CTCs in liquid biopsy, tumor metastasis, and organoid preclinical models. The study of CTCs offers broad pathways to develop new biomarkers for tumor patient diagnosis, prognosis, and response to therapy, as well as translational models accelerating oncologic drug development.
Literature
1.
2.
3.
Menzies AM, Haydu LE, Carlino MS, Azer MW, Carr PJA, Kefford RF, et al. Inter- and intra-patient heterogeneity of response and progression to targeted therapy in metastatic melanoma. PLoS ONE. 2014;9(1):e85004.PubMedPubMedCentralCrossRef
4.
De Heer EC, Brouwers AH, Boellaard R, Sluiter WJ, Diercks GFH, Hospers GAP, et al. Mapping heterogeneity in glucose uptake in metastatic melanoma using quantitative 18F-FDG PET/CT analysis. EJNMMI Res. 2018;8(1):101.PubMedPubMedCentralCrossRef
5.
Chua KLM, Yeo ELL, Shihabudeen WA, Tan SH, Shwe TT, Ong EHW, et al. Intra-patient and inter-patient comparisons of DNA damage response biomarkers in Nasopharynx Cancer (NPC): analysis of NCC0901 randomised controlled trial of induction chemotherapy in locally advanced NPC. BMC Cancer. 2018;18:1095.PubMedPubMedCentralCrossRef
6.
Dutta D, Heo I, Clevers HJ. Disease modeling in stem cell-derived 3D organoid systems. Trends Mol Med. 2017;23(5):393–410.PubMedCrossRef
7.
Crowley E, Di Nicolantonio F, Loupakis F, Bardelli A. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol. 2013;10(8):472–84.PubMedCrossRef
8.
Corcoran RB, Chabner BA. Application of cell-free DNA analysis to cancer treatment. N Engl J Med. 2018;379(18):1754–65.PubMedCrossRef
9.
Comino-Mendez I, Turner N. Predicting relapse with circulating tumor DNA analysis in lung cancer. Cancer Discov. 2017;7(12):1368–70.PubMedCrossRef
10.
Chen G, Huang AC, Zhang W, Zhang G, Wu M, Xu W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 2018;560(7718):382–6.PubMedPubMedCentralCrossRef
11.
Joosse SA, Pantel K. Tumor-educated platelets as liquid biopsy in cancer patients. Cancer Cell. 2015;28(5):552–4.PubMedCrossRef
12.
De Mattos-Arruda L, Mayor R, Ng CK, Weigelt B, Martinez-Ricarte F, Torrejon D, et al. Cerebrospinal fluid-derived circulating tumour DNA better represents the genomic alterations of brain tumours than plasma. Nat Commun. 2015;6:8839.PubMedPubMedCentralCrossRef
13.
Wang Y, Springer S, Mulvey CL, Silliman N, Schaefer J, Sausen M, et al. Detection of somatic mutations and HPV in the saliva and plasma of patients with head and neck squamous cell carcinomas. Sci Transl Med. 2015;7(293):293ra104.PubMedPubMedCentralCrossRef
14.
Kimura H, Fujiwara Y, Sone T, Kunitoh H, Tamura T, Kasahara K, et al. EGFR mutation status in tumour-derived DNA from pleural effusion fluid is a practical basis for predicting the response to gefitinib. Br J Cancer. 2006;95(10):1390–5.PubMedPubMedCentralCrossRef
15.
Reckamp KL, Melnikova VO, Karlovich C, Sequist LV, Camidge DR, Wakelee H, et al. A highly sensitive and quantitative test platform for detection of NSCLC EGFR mutations in urine and plasma. J Thorac Oncol. 2016;11(10):1690–700.PubMedCrossRef
16.
Diehl F, Schmidt K, Durkee KH, Moore KJ, Goodman SN, Shuber AP, et al. Analysis of mutations in DNA isolated from plasma and stool of colorectal cancer patients. Gastroenterology. 2008;135(2):489–98.PubMedCrossRef
17.
Zhang Z, Shiratsuchi H, Palanisamy N, Nagrath S, Ramnath N. Expanded circulating tumor cells from a patient with ALK-positive lung cancer present with EML4-ALK rearrangement along with resistance mutation and enable drug sensitivity testing: a case study. J Thorac Oncol. 2016;12:397–402.PubMedPubMedCentralCrossRef
18.
Jordan NV, Bardia A, Wittner BS, Benes C, Ligorio M, Zheng Y, et al. HER2 expression identifies dynamic functional states within circulating breast cancer cells. Nature. 2016;537(7618):102–6.PubMedPubMedCentralCrossRef
19.
Ashworth TR. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Aust Med J. 1869;14:146.
20.
Giannopoulou L, Kasimir-Bauer S, Lianidou ES. Liquid biopsy in ovarian cancer: recent advances on circulating tumor cells and circulating tumor DNA. Clin Chem Lab Med. 2018;56(2):186–97.PubMedCrossRef
21.
Soler A, Cayrefourcq L, Mazard T, Babayan A, Lamy PJ, Assou S, et al. Autologous cell lines from circulating colon cancer cells captured from sequential liquid biopsies as model to study therapy-driven tumor changes. Sci Rep. 2018;8(1):15931.PubMedPubMedCentralCrossRef
22.
Sefrioui D, Blanchard F, Toure E, Basile P, Beaussire L, Dolfus C, et al. Diagnostic value of CA19.9, circulating tumour DNA and circulating tumour cells in patients with solid pancreatic tumours. Br J Cancer. 2017;117(7):1017–25.PubMedPubMedCentralCrossRef
23.
Poudineh M, Sargent EH, Pantel K, Kelley SO. Profiling circulating tumour cells and other biomarkers of invasive cancers. Nat Biomed Eng. 2018;2(2):72–84.PubMedCrossRef
24.
Sh S. Silicone flotation: a simple quantitative method for the isolation of free-floating cancer cells from the blood. Cancer Biomark. 1959;12(3):590–5.
25.
Nagrath S, Sequist LV, Maheswaran S, Bell DW, Irimia D, Ulkus L, et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature. 2007;450(7173):1235–9.PubMedPubMedCentralCrossRef
26.
27.
O’Hara SM, Moreno JG, Zweitzig DR, Gross S, Gomella LG, Terstappen LW. Multigene reverse transcription-PCR profiling of circulating tumor cells in hormone-refractory prostate cancer. Clin Chem. 2004;50(5):826–35.PubMedCrossRef
28.
Zhang L, Ridgway LD, Wetzel MD, Ngo J, Yin W, Kumar D, et al. The identification and characterization of breast cancer CTCs competent for brain metastasis. Sci Transl Med. 2013;5(180):180ra48.PubMedCrossRef
29.
Racila E, Euhus D, Weiss AJ, Rao C, Mcconnell J, Terstappen LWMM, et al. Detection and characterization of carcinoma cells in the blood. Proc Natl Acad Sci USA. 1998;95:4589–94.PubMedCrossRefPubMedCentral
30.
Antonarakis ES, Lu C, Wang H, Luber B, Nakazawa M, Roeser JC, et al. AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer. N Engl J Med. 2014;371(11):1028–38.PubMedPubMedCentralCrossRef
31.
De Rubis G, Rajeev Krishnan S, Bebawy M. Liquid biopsies in cancer diagnosis, monitoring, and prognosis. Trends Pharmacol Sci. 2019;40(3):172–86.PubMedCrossRef
32.
Hamza B, Ng SR, Prakadan SM, Delgado FF, Chin CR, King EM, et al. Optofluidic real-time cell sorter for longitudinal CTC studies in mouse models of cancer. Proc Natl Acad Sci USA. 2019;116(6):2232–6.PubMedCrossRefPubMedCentral
33.
Antfolk M, Magnusson C, Augustsson P, Lilja H, Laurell T. Acoustofluidic, label-free separation and simultaneous concentration of rare tumor cells from white blood cells. Anal Chem. 2015;87(18):9322–8.PubMedCrossRef
34.
Abdulla A, Liu W, Gholamipour-Shirazi A, Sun J, Ding X. High-throughput isolation of circulating tumor cells using cascaded inertial focusing microfluidic channel. Anal Chem. 2018;90(7):4397–405.PubMedCrossRef
35.
Neves M, Azevedo R, Lima L, Oliveira MI, Peixoto A, Ferreira D, et al. Exploring sialyl-Tn expression in microfluidic-isolated circulating tumour cells: a novel biomarker and an analytical tool for precision oncology applications. N Biotechnol. 2019;49:77–87.PubMedCrossRef
36.
37.
Kim YR, Yoo JK, Jeong CW, Choi JW. Selective killing of circulating tumor cells prevents metastasis and extends survival. J Hematol Oncol. 2018;11(1):114.PubMedPubMedCentralCrossRef
38.
Rana K, Liesveld JL, King MR. Delivery of apoptotic signal to rolling cancer cells: a novel biomimetic technique using immobilized TRAIL and E-selectin. Biotechnol Bioeng. 2009;102(6):1692–702.PubMedCrossRef
39.
Phipps LE, Hino S, Muschel RJ. Targeting cell spreading: a method of sensitizing metastatic tumor cells to TRAIL-induced apoptosis. Mol Cancer Res. 2011;9(3):249–58.PubMedCrossRef
40.
Mitchell MJ, King MR. Fluid shear stress sensitizes cancer cells to receptor-mediated apoptosis via trimeric death receptors. New J Phys. 2013;15:015008.PubMedPubMedCentralCrossRef
41.
42.
Baccelli I, Schneeweiss A, Riethdorf S, Stenzinger A, Schillert A, Vogel V, et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat Biotechnol. 2013;31(6):539–44.PubMedCrossRef
43.
Miyamoto DT, Lee RJ, Kalinich M, LiCausi JA, Zheng Y, Chen T, et al. An RNA-based digital circulating tumor cell signature is predictive of drug response and early dissemination in prostate cancer. Cancer Discov. 2018;8(3):288–303.PubMedPubMedCentralCrossRef
44.
Sparano J, O’Neill A, Alpaugh K, Wolff AC, Northfelt DW, Dang CT, et al. Association of circulating tumor cells with late recurrence of estrogen receptor-positive breast cancer: a secondary analysis of a randomized clinical trial. JAMA Oncol. 2018;4(12):1700–6.PubMedPubMedCentralCrossRef
45.
Guo W, Sun YF, Shen MN, Ma XL, Wu J, Zhang CY, et al. Circulating tumor cells with stem-like phenotypes for diagnosis, prognosis, and therapeutic response evaluation in hepatocellular carcinoma. Clin Cancer Res. 2018;24(9):2203–13.PubMedCrossRef
46.
Zhou Q, Geng Q, Wang L, Huang J, Liao M, Li Y, et al. Value of folate receptor-positive circulating tumour cells in the clinical management of indeterminate lung nodules: a non-invasive biomarker for predicting malignancy and tumour invasiveness. EBioMedicine. 2019;41:236–43.PubMedPubMedCentralCrossRef
47.
Philips GK, Atkins M. Therapeutic uses of anti-PD-1 and anti-PD-L1 antibodies. Int Immunol. 2015;27(1):39–46.PubMedCrossRef
48.
Mazel M, Jacot W, Pantel K, Bartkowiak K, Topart D, Cayrefourcq L, et al. Frequent expression of PD-L1 on circulating breast cancer cells. Mol Oncol. 2015;9(9):1773–82.PubMedPubMedCentralCrossRef
49.
50.
Scher HI, Heller G, Molina A, Attard G, Danila DC, Jia X, et al. Circulating tumor cell biomarker panel as an individual-level surrogate for survival in metastatic castration-resistant prostate cancer. J Clin Oncol. 2015;33(12):1348–55.PubMedPubMedCentralCrossRef
51.
Li Y, Gong J, Zhang Q, Lu Z, Gao J, Li Y, et al. Dynamic monitoring of circulating tumour cells to evaluate therapeutic efficacy in advanced gastric cancer. Br J Cancer. 2016;114(2):138–45.PubMedPubMedCentralCrossRef
52.
Balakrishnan A, Koppaka D, Anand A, Deb B, Grenci G, Viasnoff V, et al. Circulating tumor cell cluster phenotype allows monitoring response to treatment and predicts survival. Sci Rep. 2019;9(1):7933.PubMedPubMedCentralCrossRef
53.
Jin MZ, Han RR, Qiu GZ, Ju XC, Lou G, Jin WL. Organoids: an intermediate modeling platform in precision oncology. Cancer Lett. 2018;414:174–80.PubMedCrossRef
54.
Lou YR, Leung AW. Next generation organoids for biomedical research and applications. Biotechnol Adv. 2018;36(1):132–49.PubMedCrossRef
55.
Gao D, Vela I, Sboner A, Iaquinta PJ, Karthaus WR, Gopalan A, et al. Organoid cultures derived from patients with advanced prostate cancer. Cell. 2014;159(1):176–87.PubMedPubMedCentralCrossRef
56.
Weeber F, van de Wetering M, Hoogstraat M, Dijkstra KK, Krijgsman O, Kuilman T, et al. Preserved genetic diversity in organoids cultured from biopsies of human colorectal cancer metastases. Proc Natl Acad Sci USA. 2015;112(43):13308–11.PubMedCrossRefPubMedCentral
57.
58.
Drost J, van Jaarsveld RH, Ponsioen B, Zimberlin C, van Boxtel R, Buijs A, et al. Sequential cancer mutations in cultured human intestinal stem cells. Nature. 2015;521(7550):43–7.PubMedCrossRef
59.
Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459(7244):262–5.PubMedCrossRef
60.
Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van den Brink S, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology. 2011;141(5):1762–72.PubMedCrossRef
61.
Bissell MJ, Hall HG, Parry G. How does the extracellular matrix direct gene expression? J Theor Biol. 1982;99(1):31–68.PubMedCrossRef
62.
Parry G, Cullen B, Kaetzel CS, Kramer R, Moss L. Regulation of differentiation and polarized secretion in mammary epithelial cells maintained in culture: extracellular matrix and membrane polarity influences. J Cell Biol. 1987;105(5):2043–51.PubMedCrossRef
63.
Lee GY, Kenny PA, Lee EH, Bissell MJ. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods. 2007;4(4):359–65.PubMedPubMedCentralCrossRef
64.
Sachs N, de Ligt J, Kopper O, Gogola E, Bounova G, Weeber F, et al. A living biobank of breast cancer organoids captures disease heterogeneity. Cell. 2018;172(1–2):373–86 e10.
65.
Huch M, Boj SF, Clevers H. Lgr5(+) liver stem cells, hepatic organoids and regenerative medicine. Regen Med. 2013;8(4):385–7.PubMedCrossRef
66.
Karthaus WR, Iaquinta PJ, Drost J, Gracanin A, van Boxtel R, Wongvipat J, et al. Identification of multipotent luminal progenitor cells in human prostate organoid cultures. Cell. 2014;159(1):163–75.PubMedPubMedCentralCrossRef
67.
68.
Boj SF, Hwang CI, Baker LA, Chio II, Engle DD, Corbo V, et al. Organoid models of human and mouse ductal pancreatic cancer. Cell. 2015;160(1–2):324–38.PubMedCrossRef
69.
Zhang L, Ridgway LD, Wetzel MD, Ngo J, Yin W, Kumar D, et al. The identification and characterization of breast cancer CTCs competent for brain metastasis. Sci Transl Med. 2013;5(180):180ra48-ra48.CrossRef
70.
Zhang Z, Shiratsuchi H, Lin J, Chen G, Reddy RM, Azizi E, et al. Expansion of CTCs from early stage lung cancer patients using a microfluidic co-culture model. Oncotarget. 2014;5(23):12383–97.PubMedPubMedCentral
71.
Fumagalli A, Drost J, Suijkerbuijk SJ, van Boxtel R, de Ligt J, Offerhaus GJ, et al. Genetic dissection of colorectal cancer progression by orthotopic transplantation of engineered cancer organoids. Proc Natl Acad Sci USA. 2017;114(12):E2357–64.PubMedCrossRefPubMedCentral
72.
Hodgkinson CL, Morrow CJ, Li Y, Metcalf RL, Rothwell DG, Trapani F, et al. Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer. Nat Med. 2014;20(8):897–903.PubMedCrossRef
73.
Boehnke K, Iversen PW, Schumacher D, Lallena MJ, Haro R, Amat J, et al. Assay establishment and validation of a high-throughput screening platform for three-dimensional patient-derived colon cancer organoid cultures. J Biomol Screen. 2016;21(9):931–41.PubMedPubMedCentralCrossRef
74.
Nabipour I, Assadi M. Precision medicine, an approach for development of the future medicine technologies. ISMJ. 2016;19:167–84.
75.
van de Wetering M, Francies HE, Francis JM, Bounova G, Iorio F, Pronk A, et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell. 2015;161(4):933–45.PubMedPubMedCentralCrossRef
76.
Zhang Z, Shiratsuchi H, Palanisamy N, Nagrath S, Ramnath N. Expanded circulating tumor cells from a patient with ALK-positive lung cancer present with EML4-ALK rearrangement along with resistance mutation and enable drug sensitivity testing: a case study. J Thorac Oncol. 2017;12(2):397–402.PubMedCrossRef
77.
Dijkstra KK, Cattaneo CM, Weeber F, Chalabi M, van de Haar J, Fanchi LF, et al. Generation of tumor-reactive T cells by co-culture of peripheral blood lymphocytes and tumor organoids. Cell. 2018;174(6):1586–98 e12.CrossRef
78.
79.
Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, Rao C, 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. 2004;10(20):6897–904.PubMedCrossRef
80.
Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 2004;351(8):781–91.PubMedCrossRef
81.
Cristofanilli M, Hayes DF, Budd GT, Ellis MJ, Stopeck A, Reuben JM, et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J Clin Oncol. 2005;23(7):1420–30.PubMedCrossRef
82.
Riethdorf S, Fritsche H, Muller V, Rau T, Schindlbeck C, Rack B, et al. Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: a validation study of the cell search system. Clin Cancer Res. 2007;13(3):920–8.PubMedCrossRef
83.
Zhang L, Riethdorf S, Wu G, Wang T, Yang K, Peng G, et al. Meta-analysis of the prognostic value of circulating tumor cells in breast cancer. Clin Cancer Res. 2012;18(20):5701–10.PubMedCrossRef
84.
Kurihara T, Itoi T, Sofuni A, Itokawa F, Tsuchiya T, Tsuji S, et al. Detection of circulating tumor cells in patients with pancreatic cancer: a preliminary result. J Hepatobiliary Pancreat Surg. 2008;15(2):189–95.PubMedCrossRef
85.
Stott SL, Lee RJ, Nagrath S, Yu M, Miyamoto DT, Ulkus L, et al. Isolation and characterization of circulating tumor cells from patients with localized and metastatic prostate cancer. Sci Transl Med. 2010;2(25):25ra3-ra3.CrossRef
86.
87.
Mohme M, Riethdorf S, Pantel K. Circulating and disseminated tumour cells—mechanisms of immune surveillance and escape. Nat Rev Clin Oncol. 2017;14(3):155–67.PubMedCrossRef
88.
Millner LM, Linder MW, Roland Valdes J. Circulating tumor cells: a review of present methods and the need to identify heterogeneous phenotypes. Ann Clin Lab Sci. 2013;43(3):2013.
89.
Martin OA, Anderson RL, Narayan K, MacManus MP. Does the mobilization of circulating tumour cells during cancer therapy cause metastasis? Nat Rev Clin Oncol. 2017;14(1):32–44.PubMedCrossRef
90.
Krishnamurthy N, Spencer E, Torkamani A, Nicholson L. Liquid biopsies for cancer: coming to a patient near you. J Clin Med. 2017;6(1):3.PubMedCentralCrossRef
91.
Joosse SA, Pantel K. Biologic challenges in the detection of circulating tumor cells. Cancer Res. 2013;73(1):8–11.PubMedCrossRef
92.
Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell. 2011;147(5):992–1009.PubMedCrossRef
93.
Camara O, Kavallaris A, Nöschel H, Rengsberger M, Jörke C, Pachmann K. Seeding of epithelial cells into circulation during surgery for breast cancer: the fate of malignant and benign mobilized cells. World J Surg Oncol. 2006;4:67.PubMedPubMedCentralCrossRef
94.
Fornvik D, Andersson I, Dustler M, Ehrnstrom R, Ryden L, Tingberg A, et al. No evidence for shedding of circulating tumor cells to the peripheral venous blood as a result of mammographic breast compression. Breast Cancer Res Treat. 2013;141(2):187–95.PubMedPubMedCentralCrossRef
95.
McDonald DM, Baluk P. Significance of blood vessel leakiness in cancer. Cancer Res. 2002;62(18):5381–5.PubMed
96.
Friedl P, Wolf K. Proteolytic interstitial cell migration: a five-step process. Cancer Metastasis Rev. 2009;28(1–2):129–35.PubMedCrossRef
97.
98.
Liotta LA, Saidel MG, Kleinerman J. The significance of hematogenous tumor cell clumps in the metastatic process. Cancer Res. 1976;36(3):889–94.PubMed
99.
Cho EH, Wendel M, Luttgen M, Yoshioka C, Marrinucci D, Lazar D, et al. Characterization of circulating tumor cell aggregates identified in patients with epithelial tumors. Phys Biol. 2012;9(1):016001.PubMedPubMedCentralCrossRef
100.
Isaiah JF. The relationship of ernbolic homogeneity, number, size and viability to the incidence of experimental metastas. Eur J Cancer. 1973;9:223–7.CrossRef
101.
Molnar B, Ladanyi A, Tanko L, Sreter L, Tulassay Z. Circulating tumor cell clusters in the peripheral blood of colorectal cancer patients. Clin Cancer Res. 2001;7(12):4080–5.PubMed
102.
Stott SL, Hsu CH, Tsukrov DI, Yu M, Miyamoto DT, Waltman BA, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Natl Acad Sci USA. 2010;107(43):18392–7.PubMedCrossRefPubMedCentral
103.
Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339(6119):580–4.PubMedPubMedCentralCrossRef
104.
Aceto N, Bardia A, Miyamoto DT, Donaldson MC, Wittner BS, Spencer JA, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell. 2014;158(5):1110–22.PubMedPubMedCentralCrossRef
105.
Cheung KJ, Padmanaban V, Silvestri V, Schipper K, Cohen JD, Fairchild AN, et al. Polyclonal breast cancer metastases arise from collective dissemination of keratin 14-expressing tumor cell clusters. Proc Natl Acad Sci USA. 2016;113(7):E854–63.PubMedCrossRefPubMedCentral
106.
Gkountela S, Castro-Giner F, Szczerba BM, Vetter M, Landin J, Scherrer R, et al. Circulating tumor cell clustering shapes DNA methylation to enable metastasis seeding. Cell. 2019;176(1–2):98–112.e14.PubMedPubMedCentralCrossRef
107.
Liu X, Taftaf R, Kawaguchi M, Chang YF, Chen W, Entenberg D, et al. Homophilic CD44 interactions mediate tumor cell aggregation and polyclonal metastasis in patient-derived breast cancer models. Cancer Discov. 2019;9(1):96–113.PubMedCrossRef
108.
Praharaj PP, Bhutiab SK, Nagrath S, Bitting RL, Gagan D. Circulating tumor cell-derived organoids: current challenges and promises in medical research and precision medicine. BBA Rev Cancer. 2018;2018:117–27.
109.
110.
111.
Van der Auwera I, Peeters D, Benoy IH, Elst HJ, Van Laere SJ, Prove A, et al. Circulating tumour cell detection: a direct comparison between the Cell Search System, the AdnaTest and CK-19/mammaglobin RT-PCR in patients with metastatic breast cancer. Br J Cancer. 2010;102(2):276–84.PubMedCrossRef
112.
Saucedo-Zeni N, Mewes S, Niestroj R, Gasiorowski L, Murawa D, Nowaczyk P, et al. A novel method for the in vivo isolation of circulating tumor cells from peripheral blood of cancer patients using a functionalized and structured medical wire. Int J Oncol. 2012;41(4):1241–50.PubMedPubMedCentral
113.
Gorges TM, Penkalla N, Schalk T, Joosse SA, Riethdorf S, Tucholski J, et al. Enumeration and molecular characterization of tumor cells in lung cancer patients using a novel in vivo device for capturing circulating tumor cells. Clin Cancer Res. 2016;22(9):2197–206.PubMedCrossRef
114.
Zhian L, Alberto F, Eva K, Alexander S, Ingeborg T, Nonnenmacher A, et al. Negative enrichment by immunomagnetic nanobeads for unbiased characterization of circulating tumor cells from peripheral blood of cancer patients. J Transl Med. 2011;9:70.CrossRef
115.
Harb W, Fan A, Tran T, Danila DC, Keys D, Schwartz M, et al. Mutational analysis of circulating tumor cells using a novel microfluidic collection device and qPCR assay. Transl Oncol. 2013;6(5):528–38.PubMedPubMedCentralCrossRef
116.
Chinen LT, de Carvalho FM, Rocha BM, Aguiar CM, Abdallah EA, Campanha D, et al. Cytokeratin-based CTC counting unrelated to clinical follow up. J Thorac Dis. 2013;5(5):593–9.PubMedPubMedCentral
117.
Harouaka RA, Nisic M, Zheng SY. Circulating tumor cell enrichment based on physical properties. J Lab Autom. 2013;18(6):455–68.PubMedCrossRef
118.
Wan Y, Winter M, Delalat B, Hardingham JE, Grover PK, Wrin J, et al. Nanostructured polystyrene well plates allow unbiased high-throughput characterization of circulating tumor cells. ACS Appl Mater Interfaces. 2014;6(23):20828–36.PubMedCrossRef
119.
Riahi R, Gogoi P, Sepehri S, Zhou Y, Handique K, Godsey J, et al. A novel microchannel-based device to capture and analyze circulating tumor cells (CTCs) of breast cancer. Int J Oncol. 2014;44(6):1870–8.PubMedPubMedCentralCrossRef
120.
121.
Waheed W, Alazzam A, Mathew B, Christoforou N, Abu-Nada E. Lateral fluid flow fractionation using dielectrophoresis (LFFF-DEP) for size-independent, label-free isolation of circulating tumor cells. J Chromatogr B Analyt Technol Biomed Life Sci. 2018;1087–1088:133–7.PubMedCrossRef
122.
De Luca F, Rotunno G, Salvianti F, Galardi F, Pestrin M, Gabellini S, et al. Mutational analysis of single circulating tumor cells by next generation sequencing in metastatic breast cancer. Oncotarget. 2016;7(18):26107–19.PubMedPubMedCentral
123.
Tulley S, Zhao Q, Dong H, Pearl ML, Chen WT. Vita-assay method of enrichment and identification of circulating cancer cells/circulating tumor cells (CTCs). Methods Mol Biol. 2016;1406:107–19.PubMedCrossRef
124.
Alix-Panabieres C. EPISPOT assay: detection of viable DTCs/CTCs in solid tumor patients. Recent Results Cancer Res. 2012;195:69–76.PubMedCrossRef
125.
Togo S, Katagiri N, Namba Y, Tulafu M, Nagahama K, Kadoya K, et al. Sensitive detection of viable circulating tumor cells using a novel conditionally telomerase-selective replicating adenovirus in non-small cell lung cancer patients. Oncotarget. 2017;8(21):34884–95.PubMedPubMedCentralCrossRef
126.
Powell AA, Talasaz AH, Zhang H, Coram MA, Reddy A, Deng G, et al. Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines. PLoS ONE. 2012;7(5):e33788.PubMedPubMedCentralCrossRef
127.
Giordano A, Gao H, Anfossi S, Cohen E, Mego M, Lee BN, et al. Epithelial-mesenchymal transition and stem cell markers in patients with HER2-positive metastatic breast cancer. Mol Cancer Ther. 2012;11(11):2526–34.PubMedPubMedCentralCrossRef
128.
Smirnov DA, Zweitzig DR, Foulk BW, Miller MC, Doyle GV, Pienta KJ, et al. Global gene expression profiling of circulating tumor cells. Cancer Res. 2005;65(12):4993–7.PubMedCrossRef
129.
Pestrin M, Bessi S, Puglisi F, Minisini AM, Masci G, Battelli N, et al. Final results of a multicenter phase II clinical trial evaluating the activity of single-agent lapatinib in patients with HER2-negative metastatic breast cancer and HER2-positive circulating tumor cells. A proof-of-concept study. Breast Cancer Res Treat. 2012;134(1):283–9.PubMedCrossRef
130.
Kalykaki A, Agelaki S, Kallergi G, Xyrafas A, Mavroudis D, Georgoulias V. Elimination of EGFR-expressing circulating tumor cells in patients with metastatic breast cancer treated with gefitinib. Cancer Chemother Pharmacol. 2014;73(4):685–93.PubMedCrossRef
131.
Kallergi G, Agelaki S, Kalykaki A, Stournaras C, Mavroudis D, Georgoulias V. Phosphorylated EGFR and PI3K/Akt signaling kinases are expressed in circulating tumor cells of breast cancer patients. Breast Cancer Res. 2008;10(5):R80.PubMedPubMedCentralCrossRef
132.
Mostert B, Jiang Y, Sieuwerts AM, Wang H, Bolt-de Vries J, Biermann K, et al. KRAS and BRAF mutation status in circulating colorectal tumor cells and their correlation with primary and metastatic tumor tissue. Int J Cancer. 2013;133(1):130–41.PubMedCrossRef
133.
Paoletti C, Larios JM, Muñiz MC, Aung K, Cannell EM, Darga EP, et al. Heterogeneous estrogen receptor expression in circulating tumor cells suggests diverse mechanisms of fulvestrant resistance. Mol Oncol. 2016;10(7):1078–85.PubMedPubMedCentralCrossRef
134.
Kuhlmann JD, Wimberger P, Bankfalvi A, Keller T, Scholer S, Aktas B, et al. ERCC1-positive circulating tumor cells in the blood of ovarian cancer patients as a predictive biomarker for platinum resistance. Clin Chem. 2014;60(10):1282–9.PubMedCrossRef
Metadata
Title
Circulating tumor cells in precision oncology: clinical applications in liquid biopsy and 3D organoid model
Authors
Chang Yang
Bai-Rong Xia
Wei-Lin Jin
Ge Lou
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Metastasis
Published in
Cancer Cell International / Issue 1/2019
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-019-1067-8

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