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      Epithelial-type systemic breast carcinoma cells with a restricted mesenchymal transition are a major source of metastasis

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          Abstract

          Association of epithelial-mesenchymal transition with the metastatic potential of disseminated cells in breast cancer was studied.

          Abstract

          Carcinoma cells undergo epithelial-mesenchymal transition (EMT); however, contributions of EMT heterogeneity to disease progression remain a matter of debate. Here, we addressed the EMT status of ex vivo cultured circulating and disseminated tumor cells (CTCs/DTCs) in a syngeneic mouse model of metastatic breast cancer (MBC). Epithelial-type CTCs with a restricted mesenchymal transition had the strongest lung metastases formation ability, whereas mesenchymal-type CTCs showed limited metastatic ability. EpCAM expression served as a surrogate marker to evaluate the EMT heterogeneity of clinical samples from MBC, including metastases, CTCs, and DTCs. The proportion of epithelial-type CTCs, and especially DTCs, correlated with distant metastases and poorer outcome of patients with MBC. This study fosters our understanding of EMT in metastasis and underpins heterogeneous EMT phenotypes as important parameters for tumor prognosis and treatment. We further suggest that EpCAM-dependent CTC isolation systems will underestimate CTC numbers but will quantify clinically relevant metastatic cells.

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          Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor.

          C Aslakson, F R Miller (1992)
          To identify selective steps in metastasis, those that eliminate nonmetastatic tumor cells more efficiently than metastatic cells, we have evaluated the sequential dissemination of tumor cells from a mammary fatpad, using both metastatic (4T1 and 66cl4) and nonmetastatic (67NR, 168FARN, and 4TO7) subpopulations of a single mouse mammary tumor. Each of these variant subpopulations is resistant to one or more selective drugs so they could be quantitatively identified by colony formation in selective media. We found that the 2 metastatic cell lines metastasized by different routes and that the nonmetastatic tumor cell lines failed at different points in dissemination. Line 67NR did not leave the primary site; clonogenic tumor cells were not detected in the nodes, blood, or lungs during the experiment (7 weeks). Tumor line 168FARN disseminated from the primary tumor because clonogenic cells were cultured from the draining lymph nodes throughout the experiment. However, dissemination essentially stopped in the node as cells were rarely isolated from blood, lungs, or lives. Whether 168FARN cells failed to reach these tissues or were killed very rapidly after traversing the lymph node is unknown. Line 4TO7 cells disseminated via the blood and were consistently recovered from lungs by day 19 but failed to proliferate. This panel of 5 subpopulations thus identifies different points of selective failure in tumor cell dissemination and should be valuable in the assessment of antimetastatic therapies.
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            Epithelial-mesenchymal transition spectrum quantification and its efficacy in deciphering survival and drug responses of cancer patients

            Tuan Tan, Qing Hao Miow, Yoshio Miki … (2014)
            Epithelial-mesenchymal transition (EMT) is a reversible and dynamic process hypothesized to be co-opted by carcinoma during invasion and metastasis. Yet, there is still no quantitative measure to assess the interplay between EMT and cancer progression. Here, we derived a method for universal EMT scoring from cancer-specific transcriptomic EMT signatures of ovarian, breast, bladder, lung, colorectal and gastric cancers. We show that EMT scoring exhibits good correlation with previously published, cancer-specific EMT signatures. This universal and quantitative EMT scoring was used to establish an EMT spectrum across various cancers, with good correlation noted between cell lines and tumours. We show correlations between EMT and poorer disease-free survival in ovarian and colorectal, but not breast, carcinomas, despite previous notions. Importantly, we found distinct responses between epithelial- and mesenchymal-like ovarian cancers to therapeutic regimes administered with or without paclitaxelin vivo and demonstrated that mesenchymal-like tumours do not always show resistance to chemotherapy. EMT scoring is thus a promising, versatile tool for the objective and systematic investigation of EMT roles and dynamics in cancer progression, treatment response and survival.
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              Biology, detection, and clinical implications of circulating tumor cells

              Simon Joosse, Tobias Gorges, Klaus Pantel (2014)
              Cancer metastasis is the main cause of cancer-related death, and dissemination of tumor cells through the blood circulation is an important intermediate step that also exemplifies the switch from localized to systemic disease. Early detection and characterization of circulating tumor cells (CTCs) is therefore important as a general strategy to monitor and prevent the development of overt metastatic disease. Furthermore, sequential analysis of CTCs can provide clinically relevant information on the effectiveness and progression of systemic therapies (e.g., chemo-, hormonal, or targeted therapies with antibodies or small inhibitors). Although many advances have been made regarding the detection and molecular characterization of CTCs, several challenges still exist that limit the current use of this important diagnostic approach. In this review, we discuss the biology of tumor cell dissemination, technical advances, as well as the challenges and potential clinical implications of CTC detection and characterization.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Sci Adv
                Journal ID (iso-abbrev): Sci Adv
                Journal ID (publisher-id): SciAdv
                Journal ID (hwp): advances
                Title: Science Advances
                Publisher: American Association for the Advancement of Science
                ISSN (Electronic): 2375-2548
                Publication date Collection: June 2019
                Publication date (Electronic): 19 June 2019
                Volume: 5
                Issue: 6
                Electronic Location Identifier: eaav4275
                Affiliations
                [1 ]Department of Otorhinolaryngology, Head and Neck Surgery, University Hospital, Ludwig-Maximilians University of Munich, Marchioninistr. 15, 81377 Munich, Germany.
                [2 ]Department of Oncology, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200080, China.
                [3 ]Center of Integrated Protein Science Munich and Division of Clinical Pharmacology, Department of Medicine IV, Klinikum der Ludwig-Maximilians-Universität München, Member of the German Center for Lung Research, Lindwurmstrasse 2a, 80337 Munich, Germany.
                [4 ]Cytelligen, San Diego, CA 92121, USA.
                [5 ]Department of Epidemiology and Biostatistics, School of Public Health, Nanjing Medical University, Nanjing 211166, China.
                [6 ]Clinical Cooperation Group Personalized Radiotherapy of Head and Neck Tumors, Helmholtz Zentrum München, Neuherberg, Germany.
                [7 ]Research Unit Radiation Cytogenetics, Helmholtz Zentrum München, Neuherberg, Germany.
                [8 ]Department of Radiation Oncology, University Hospital, LMU Munich, Munich, Germany.
                [9 ]State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, China.
                Author notes
                [*]

                These authors contributed equally to this work.

                [†]

                These authors contributed equally to this work as senior authors.

                [‡ ]Corresponding author. Email: olivier.gires@ 123456med.uni-muenchen.de (O.G.); whx365@ 123456126.com (H.W.)
                Author information
                http://orcid.org/0000-0001-7045-3898
                http://orcid.org/0000-0002-5612-4673
                http://orcid.org/0000-0002-2292-7064
                Article
                Publisher ID: aav4275
                DOI: 10.1126/sciadv.aav4275
                PMC ID: 6584608
                PubMed ID: 31223646
                SO-VID: 8bf918b1-9ee1-465f-aac7-21e37a410a7c
                Copyright © Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                Date received : 14 September 2018
                Date accepted : 15 May 2019
                Funding
                Funded by: doi http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: GI 540/3-1
                Funded by: doi http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: GI 540/3-1
                Funded by: ERC Starting Grant;
                Award ID: 756017
                Funded by: Shanghai Science and Technology Innovation Action Plan;
                Award ID: 16ZR1427400
                Funded by: Elite Network of Bavaria;
                Funded by: Marie-Sklodowska-Curie H2020 program European Union;
                Funded by: China National Natural Science Funds;
                Award ID: 81772802
                Categories
                Subject: Research Article
                Subject: Research Articles
                Subject: SciAdv r-articles
                Subject: Cancer
                Subject: Cancer
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                Copyeditor Jeanelle Ebreo

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