Dissemination and Characteristics of Circulating Tumor Cells in Breast Cancer: Comparison
View Latest Version
Please note this is a comparison between Version 5 by Nicole Yin and Version 6 by Rita Xu.

Breast cancer metastasis is the leading cause of cancer deaths in women and is difficult to combat due to the long periods in which disseminated cells stay dormant and can be re-activated to start the relapse. Assessing the number and molecular profile of circulating tumor cells (CTCs) in breast cancer patients, especially in early breast cancer, should help in identifying the possibility of relapse in time for therapeutic intervention to prevent or delay recurrence. Molecular analysis of CTCs have a potential to define particular susceptibilities of the cells representing the current tumor burden, which may be considerably different from the cells of the primary tumor. While metastatic breast cancer is considered incurable this approach may off er more tailored therapy to the patients. In this article we inspect the routes to metastasis in breast cancer and how they can be linked to specific features of CTCs, how CTC analysis may be used in therapy, and what is the current status of the research and efforts to include CTC analysis in clinical practice.

  • CTC
  • breast cancer
  • metastasis
Please wait, diff process is still running!

References

  1. Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A; Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2018, 68, 394–424.
  2. Szostakowska, M.; Trebinska-Stryjewska, A.; Grzybowska, E.A.; Fabisiewicz, A; Resistance to endocrine therapy in breast cancer: Molecular mechanisms and future goals. Breast Cancer Res. Treat. 2019, 173, 489–497, 10.1038/nrc2627.
  3. Demicheli, R.; Ardoino, I.; Boracchi, P.; Coradini, D.; Agresti, R.; Ferraris, C.; Gennaro, M.; Hrushesky, W.J.; Biganzoli, E. Recurrence and mortality according to estrogen receptor status for breast cancer patients undergoing conservative surgery. Ipsilateral breast tumour recurrence dynamics provides clues for tumour biology within the residual breast. BMC Cancer 2010, 10, 656.
  4. Liedtke, C.; Mazouni, C.; Hess, K.R.; Andre, F.; Tordai, A.; Mejia, J.A.; Symmans, W.F.; Gonzalez-Angulo, A.M.; Hennessy, B.; Green, M.; et al.et al Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J. Clin. Oncol. 2008, 26, 1275–1281, 10.1016/s0093-7754(02)70065-1.
  5. Dent, R.; Trudeau, M.; Pritchard, K.I.; Hanna, W.M.; Kahn, H.K.; Sawka, C.A.; Lickley, L.A.; Rawlinson, E.; Sun, P.; Narod, S.A; et al. Triple-negative breast cancer: Clinical features and patterns of recurrence. Clin. Cancer Res. 2007, 13, 4429–4434.
  6. Klein, C.A.; Holzel, D; Systemic cancer progression and tumor dormancy: Mathematical models meet single cell genomics. Cell Cycle 2006, 5, 1788–1798.
  7. Klein, C.A; Parallel progression of primary tumours and metastases. Nat. Rev. Cancer 2009, 9, 302–312.
  8. Bockhorn, M.; Jain, R.K.; Munn, L.L; Active versus passive mechanisms in metastasis: Do cancer cells crawl into vessels, or are they pushed?. Lancet Oncol 2007, 8, 444–448, 10.1038/srep43813.
  9. Judah Folkman; Role of angiogenesis in tumor growth and metastasis. Seminars in Oncology 2002, 29, 15-18, 10.1016/s0093-7754(02)70065-1.
  10. Gerhard Hamilton; Barbara Rath; Circulating Tumor Cells in the Parallel Invasion Model Supporting Early Metastasis. Oncomedicine 2018, 3, 15-27, 10.7150/oncm.22576.
  11. Hosseini, H.; Obradovic, M.M.S.; Hoffmann, M.; Harper, K.L.; Sosa, M.S.; Werner-Klein, M.; Nanduri, L.K.; Werno, C.; Ehrl, C.; Maneck, M; et al. Early dissemination seeds metastasis in breast cancer. Nature 2016, 540, 552-558, 10.1038/nature20785.
  12. Harper, K.L.; Sosa, M.S.; Entenberg, D.; Hosseini, H.; Cheung, J.F.; Nobre, R.; Avivar-Valderas, A.; Nagi, C.; Girnius, N.; Davis, R.J; et al. Mechanism of early dissemination and metastasis in Her2+ mammary cancer. Nature 2016, 540, 588-592, 10.1038/nature20609.
  13. Kroigard, A.B.; Larsen, M.J.; Brasch-Andersen, C.; Laenkholm, A.V.; Knoop, A.S.; Jensen, J.D.; Bak, M.; Mollenhauer, J.; Thomassen, M.; Kruse, T.A; et al. Genomic Analyses of Breast Cancer Progression Reveal Distinct Routes of Metastasis Emergence. Scientific Reports 2017, 7, 43813, 10.1038/srep43813.
  14. Tan, T.Z.; Miow, Q.H.; Miki, Y.; Noda, T.; Mori, S.; Huang, R.Y.; Thiery, J.P; Epithelial‐mesenchymal transition spectrum quantification and its efficacy in deciphering survival and drug responses of cancer patients. EMBO Molecular Medicine 2014, 6, 1279-1293, 10.15252/emmm.201404208.
  15. Fischer, K.R.; Durrans, A.; Lee, S.; Sheng, J.; Li, F.; Wong, S.T.; Choi, H.; El Rayes, T.; Ryu, S.; Troeger, J; et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 2015, 527, 472-476, 10.1038/nature15748.
  16. Ye, X.; Brabletz, T.; Kang, Y.; Longmore, G.D.; Nieto, M.A.; Stanger, B.Z.; Yang, J.; Weinberg, R.A. Upholding a role for EMT in breast cancer metastasis. Nature 2017, 547, E1–E3.
  17. Frank A. W. Coumans; S. Siesling; Leon W.M.M. Terstappen; Detection of cancer before distant metastasis. BMC Cancer 2013, 13, 283, 10.1186/1471-2407-13-283.
  18. Peeters, D.J.; van Dam, P.J.; Van den Eynden, G.G.; Rutten, A.; Wuyts, H.; Pouillon, L.; Peeters, M.; Pauwels, P.; Van Laere, S.J.; van Dam, P.A; et al. Detection and prognostic significance of circulating tumour cells in patients with metastatic breast cancer according to immunohistochemical subtypes. British Journal of Cancer 2013, 110, 375-383, 10.1038/bjc.2013.743.
  19. Nicola Aceto; Fluctuating numbers of circulating tumor cells in cancer patients and the meaning of zero counts.. Oncotarget 2019, 10, 2658-2659, 10.18632/oncotarget.26850.
  20. Marta Vilalta; Marjan Rafat; Amato J. Giaccia; Edward E. Graves; Recruitment of circulating breast cancer cells is stimulated by radiotherapy.. Cell Reports 2014, 8, 402-409, 10.1016/j.celrep.2014.06.011.
  21. Martin, O.A.; Anderson, R.L.; Narayan, K.; MacManus, M.P; Does the mobilization of circulating tumour cells during cancer therapy cause metastasis?. Nat. Rev. Clin. Oncol. 2017, 14, 32–44.
  22. Vetter, M.; Landin, J.; Szczerba, B.M.; Castro-Giner, F.; Gkountela, S.; Donato, C.; Krol, I.; Scherrer, R.; Balmelli, C.; Malinovska, A.; et al.et al. Denosumab treatment is associated with the absence of circulating tumor cells in patients with breast cancer. Breast Cancer Research 2018, 20, 141, 10.1186/s13058-018-1067-y.
  23. Shaw, J.A.; Guttery, D.S.; Hills, A.; Fernandez-Garcia, D.; Page, K.; Rosales, B.M.; Goddard, K.S.; Hastings, R.K.; Luo, J.; Ogle, O.; et al. Mutation analysis of cell-free DNA and single circulating tumor cells in metastatic breast cancer patients with high CTC counts. Clinical Cancer Research 2017, 23, 88-96, 10.1158/1078-0432.CCR-16-0825.
  24. Qi Wang; Lanbo Zhao; Lu Han; Xiaoqian Tuo; Sijia Ma; Yiran Wang; Xue Feng; Dongxin Liang; Chao Sun; Qing Wang; et al.Qing SongQiling Li The Discordance of Gene Mutations between Circulating Tumor Cells and Primary/Metastatic Tumor. Molecular Therapy - Oncolytics 2019, 15, 21-29, 10.1016/j.omto.2019.08.006.
  25. Marta Pestrin; Francesca Salvianti; Francesca Galardi; Francesca De Luca; Natalie Turner; Luca Malorni; Mario Pazzagli; Angelo Di Leo; Pamela Pinzani; Heterogeneity of PIK3CA mutational status at the single cell level in circulating tumor cells from metastatic breast cancer patients. Molecular Oncology 2015, 9, 749-757, 10.1016/j.molonc.2014.12.001.
  26. De Luca, F.; Rotunno, G.; Salvianti, F.; Galardi, F.; Pestrin, M.; Gabellini, S.; Simi, L.; Mancini, I.; Vannucchi, A.M.; Pazzagli, M.; et al. Mutational analysis of single circulating tumor cells by next generation sequencing in metastatic breast cancer. Oncotarget 2016, 7, 26107–26119.
  27. Yu, M.; Bardia, A.; Aceto, N.; Bersani, F.; Madden, M.W.; Donaldson, M.C.; Desai, R.; Zhu, H.; Comaills, V.; Zheng, Z.; et al.et al Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 2014, 345, 216–220, 10.1016/j.molonc.2015.05.009.
  28. Aktas, B.; Muller, V.; Tewes, M.; Zeitz, J.; Kasimir-Bauer, S.; Loehberg, C.R.; Rack, B.; Schneeweiss, A.; Fehm, T; Comparison of estrogen and progesterone receptor status of circulating tumor cells and the primary tumor in metastatic breast cancer patients. Gynecol. Oncol. 2011, 122, 356–360.
  29. Aktas, B.; Kasimir-Bauer, S.; Muller, V.; Janni, W.; Fehm, T.; Wallwiener, D.; Pantel, K.; Tewes, M.; Group, D.S. Comparison of the HER2, estrogen and progesterone receptor expression profile of primary tumor, metastases and circulating tumor cells in metastatic breast cancer patients. BMC Cancer 2016, 16, 522.
  30. S. M. Frisch; H Francis; Disruption of epithelial cell-matrix interactions induces apoptosis. Journal of Cell Biology 1994, 124, 619-626, 10.1083/jcb.124.4.619.
  31. Luzzi, K.J.; MacDonald, I.C.; Schmidt, E.E.; Kerkvliet, N.; Morris, V.L.; Chambers, A.F.; Groom, A.C; Multistep nature of metastatic inefficiency: Dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 1998, 153, 865–873.
  32. Martine Mazel; William Jacot; Klaus Pantel; Kai Bartkowiak; Delphine Topart; Laure Cayrefourcq; Delphine Rossille; Thierry Maudelonde; Thierry Fest; Catherine Alix-Panabières; et al. Frequent expression of PD‐L1 on circulating breast cancer cells. Molecular Oncology 2015, 9, 1773-1782, 10.1016/j.molonc.2015.05.009.
  33. Brisotto, G.; Biscontin, E.; Rossi, E.; Bulfoni, M.; Piruska, A.; Spazzapan, S.; Poggiana, C.; Vidotto, R.; Steffan, A.; Colombatti, A.; et al.et al Dysmetabolic circulating tumor cells are prognostic in Metastatic Breast Cancer. medRxiv 2019, null, null.
  34. LeBleu, V.S.; O’Connell, J.T.; Gonzalez Herrera, K.N.; Wikman, H.; Pantel, K.; Haigis, M.C.; de Carvalho, F.M.; Damascena, A.; Domingos Chinen, L.T.; Rocha, R.M.; et al.et al PGC-1alpha mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat. Cell Biol. 2014, 16, 992–1003.
  35. Baccelli, I.; Schneeweiss, A.; Riethdorf, S.; Stenzinger, A.; Schillert, A.; Vogel, V.; Klein, C.; Saini, M.; Bauerle, T.; Wallwiener, M.; et al.et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nature Biotechnology 2013, 31, 539-544, 10.1038/nbt.2576.
  36. Areti Strati; Michail Nikolaou; Vassilis Georgoulias; Evi S. Lianidou; Prognostic Significance of TWIST1, CD24, CD44, and ALDH1 Transcript Quantification in EpCAM-Positive Circulating Tumor Cells from Early Stage Breast Cancer Patients. Cells 2019, 8, 652, 10.3390/cells8070652.
  37. Reijm, E.A.; Sieuwerts, A.M.; Smid, M.; Vries, J.B.; Mostert, B.; Onstenk, W.; Peeters, D.; Dirix, L.Y.; Seynaeve, C.M.; Jager, A.; et al.et al. An 8-gene mRNA expression profile in circulating tumor cells predicts response to aromatase inhibitors in metastatic breast cancer patients.. BMC Cancer 2016, 16, 123, 10.1186/s12885-016-2155-y.
  38. Bredemeier, M.; Edimiris, P.; Mach, P.; Kubista, M.; Sjoback, R.; Rohlova, E.; Kolostova, K.; Hauch, S.; Aktas, B.; Tewes, M.; et al.et al. Gene Expression Signatures in Circulating Tumor Cells Correlate with Response to Therapy in Metastatic Breast Cancer. Clinical Chemistry 2017, 63, 1585-1593, 10.1373/clinchem.2016.269605.
  39. Kristina E. Aaltonen; Vendula Novosadova; Pär-Ola Bendahl; Cecilia Graffman; Anna-Maria Larsson; Lisa Rydén; Molecular characterization of circulating tumor cells from patients with metastatic breast cancer reflects evolutionary changes in gene expression under the pressure of systemic therapy. Oncotarget 2017, 8, 45544-45565, 10.18632/oncotarget.17271.
  40. de Wit, S.; Manicone, M.; Rossi, E.; Lampignano, R.; Yang, L.; Zill, B.; Rengel-Puertas, A.; Ouhlen, M.; Crespo, M.; Berghuis, A.M.S.; et al. EpCAM(high) and EpCAM(low) circulating tumor cells in metastatic prostate and breast cancer patients. Oncotarget 2018, 9, 35705–35716.
  41. Padmanaban, V.; Krol, I.; Suhail, Y.; Szczerba, B.M.; Aceto, N.; Bader, J.S.; Ewald, A.J. E-cadherin is required for metastasis in multiple models of breast cancer. Nature 2019, 573, 439–444.
  42. Thiery, J.P.; Acloque, H.; Huang, R.Y.; Nieto, M.A; Epithelial-mesenchymal transitions in development and disease. Cell 2010, 139, 871–890.
  43. Mohini Singh; Nicolas Yelle; Chitra Venugopal; Sheila K. Singh; EMT: Mechanisms and therapeutic implications. Pharmacology & Therapeutics 2018, 182, 80-94, 10.1016/j.pharmthera.2017.08.009.
  44. Zeisberg, M.; Neilson, E.G; Biomarkers for epithelial-mesenchymal transitions. J. Clin. Invest. 2019, 119, 1429–1437.
  45. Ruben Bill; Gerhard Christofori; The relevance of EMT in breast cancer metastasis: Correlation or causality?. FEBS Letters 2015, 589, 1577-1587, 10.1016/j.febslet.2015.05.002.
  46. Henrieta Skovierova; Terézia Okajčeková; Ján Strnádel; Eva Vidomanová; Erika Halašová; Molecular regulation of epithelial-to-mesenchymal transition in tumorigenesis (Review). International Journal of Molecular Medicine 2018, 41, 1187-1200, 10.3892/ijmm.2017.3320.
  47. Lamouille, S.; Xu, J.; Derynck, R; Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 2014, 15, 178–196.
  48. Jing Yang; Sendurai A Mani; Joana Liu Donaher; Sridhar Ramaswamy; Raphael A Itzykson; Christophe Come; Pierre Savagner; Inna Gitelman; Andrea Richardson; Robert A Weinberg; et al. Twist, a Master Regulator of Morphogenesis, Plays an Essential Role in Tumor Metastasis. Cell 2004, 117, 927-939, 10.1016/j.cell.2004.06.006 [doi] S0092867404005768 [pii].
  49. Spaderna, S.; Schmalhofer, O.; Wahlbuhl, M.; Dimmler, A.; Bauer, K.; Sultan, A.; Hlubek, F.; Jung, A.; Strand, D.; Eger, A.; et al.et al The Transcriptional Repressor ZEB1 Promotes Metastasis and Loss of Cell Polarity in Cancer. Cancer Research 2008, 68, 537-544, 10.1158/0008-5472.can-07-5682.
  50. Krebs, A.M.; Mitschke, J.; Lasierra Losada, M.; Schmalhofer, O.; Boerries, M.; Busch, H.; Boettcher, M.; Mougiakakos, D.; Reichardt, W.; Bronsert, P.; et al.et al The EMT-activator Zeb1 is a key factor for cell plasticity and promotes metastasis in pancreatic cancer. Nature 2017, 19, 518-529, 10.1038/ncb3513.
  51. Pastushenko, I.; Brisebarre, A.; Sifrim, A.; Fioramonti, M.; Revenco, T.; Boumahdi, S.; Van Keymeulen, A.; Brown, D.; Moers, V.; Lemaire, S.; et al.et al Identification of the tumour transition states occurring during EMT. Nature 2018, 556, 463-468.
  52. Mohit Kumar Jolly; Satyendra Tripathi; Dongya Jia; Steven M. Mooney; Muge Celiktas; Samir M. Hanash; Sendurai A. Mani; Kenneth J. Pienta; Eshel Ben-Jacob; Herbert Levine; et al. Stability of the hybrid epithelial/mesenchymal phenotype. Oncotarget 2016, 7, 27067-27084, 10.18632/oncotarget.8166.
  53. Elizabeth Williams; Dingcheng Gao; Andrew Redfern; Erik Walter Thompson; Controversies around epithelial-mesenchymal plasticity in cancer metastasis. Nature Reviews Cancer 2019, 19, 716-732, 10.1038/s41568-019-0213-x.
  54. Arthur W. Lambert; Diwakar Pattabiraman; Robert A. Weinberg; Emerging Biological Principles of Metastasis. Cell 2017, 168, 670-691, 10.1016/j.cell.2016.11.037.
  55. Tian, X.J.; Zhang, H.; Xing, J; Coupled reversible and irreversible bistable switches underlying TGFbeta-induced epithelial to mesenchymal transition. Biophys. J. 2013, 105, 1079–1089.
  56. Jolly, M.K.; Boareto, M.; Huang, B.; Jia, D.; Lu, M.; Ben-Jacob, E.; Onuchic, J.N.; Levine, H; Implications of the Hybrid Epithelial/Mesenchymal Phenotype in Metastasis. Frontiers in Oncology 2015, 5, 155, 10.3389/fonc.2015.00155.
  57. Aigner, K.; Dampier, B.; Descovich, L.; Mikula, M.; Sultan, A.; Schreiber, M.; Mikulits, W.; Brabletz, T.; Strand, D.; Obrist, P.; et al.et al The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 2007, 26, 6979–6988, 10.1126/sciadv.aav4275.
  58. Yu, M.; Bardia, A.; Wittner, B.S.; Stott, S.L.; Smas, M.E.; Ting, D.T.; Isakoff, S.J.; Ciciliano, J.C.; Wells, M.N.; Shah, A.M.; et al.et al Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013, 339, 580–584.
  59. Masao Saitoh; Involvement of partial EMT in cancer progression. The Journal of Biochemistry 2018, 164, 257-264, 10.1093/jb/mvy047.
  60. Bulfoni, M.; Gerratana, L.; Del Ben, F.; Marzinotto, S.; Sorrentino, M.; Turetta, M.; Scoles, G.; Toffoletto, B.; Isola, M.; Beltrami, C.A.; et al.et al. In patients with metastatic breast cancer the identification of circulating tumor cells in epithelial-to-mesenchymal transition is associated with a poor prognosis. Breast Cancer Res. 2016, 18, 30.
  61. Michal Mego; Marian Karaba; Gabriel Minarik; Juraj Benca; Jurisova Silvia; Tatiana Sedlackova; Denisa Manasova; Katarina Kalavska; Daniel Pindak; Massimo Cristofanilli; et al.James M. ReubenJozef Mardiak Circulating Tumor Cells With Epithelial-to-mesenchymal Transition Phenotypes Associated With Inferior Outcomes in Primary Breast Cancer. Anticancer Research 2019, 39, 1829-1837, 10.21873/anticanres.13290.
  62. Liu, X.; Li, J.; Cadilha, B.L.; Markota, A.; Voigt, C.; Huang, Z.; Lin, P.P.; Wang, D.D.; Dai, J.; Kranz, G.; et al.et al Epithelial-type systemic breast carcinoma cells with a restricted mesenchymal transition are a major source of metastasis. Sci. Adv. 2019, 5, eaav4275.
  63. Maria A. Papadaki; Giannis Stoupis; Panayiotis A. Theodoropoulos; Dimitris Mavroudis; Vassilis Georgoulias; Sofia Agelaki; Circulating Tumor Cells with Stemness and Epithelial-to-Mesenchymal Transition Features Are Chemoresistant and Predictive of Poor Outcome in Metastatic Breast Cancer. Molecular Cancer Therapeutics 2018, 18, 437-447, 10.1158/1535-7163.mct-18-0584.
  64. Evgeniya V Kaigorodova; Olga Savelieva; Liubov A. Tashireva; Natalia A. Tarabanovskaya; Elena I. Simolina; Evgeny V. Denisov; Elena M. Slonimskaya; Evgeny Choynzonov; Vladimir M. Perelmuter; Heterogeneity of Circulating Tumor Cells in Neoadjuvant Chemotherapy of Breast Cancer. Molecules 2018, 23, 727, 10.3390/molecules23040727.
  65. Guan, X.; Ma, F.; Li, C.; Wu, S.; Hu, S.; Huang, J.; Sun, X.; Wang, J.; Luo, Y.; Cai, R; et al. The prognostic and therapeutic implications of circulating tumor cell phenotype detection based on epithelial-mesenchymal transition markers in the first-line chemotherapy of HER2-negative metastatic breast cancer. Cancer Commun. (Lond) 2019, 39, 1.
  66. Wang, C.; Mu, Z.; Chervoneva, I.; Austin, L.; Ye, Z.; Rossi, G.; Palazzo, J.P.; Sun, C.; Abu-Khalaf, M.; Myers, R.E.; et al.et al Longitudinally collected CTCs and CTC-clusters and clinical outcomes of metastatic breast cancer. Breast Cancer Res. Treat. 2017, 161, 83-94, 10.1007/s10549-016-4026-2.
  67. Aleksandra Markiewicz; Justyna Topa; Anna Nagel; Jarosław Skokowski; Barbara Seroczynska; Tomasz Stokowy; Marzena Welnicka-Jaskiewicz; Anna J. Zaczek; Spectrum of Epithelial-Mesenchymal Transition Phenotypes in Circulating Tumour Cells from Early Breast Cancer Patients. Cancers 2019, 11, 59, 10.3390/cancers11010059.
  68. Aceto, N.; Bardia, A.; Miyamoto, D.T.; Donaldson, M.C.; Wittner, B.S.; Spencer, J.A.; Yu, M.; Pely, A.; Engstrom, A.; Zhu, H.; et al.et al Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 2014, 158, 1110-1122.
  69. Cheung, K.J.; Padmanaban, V.; Silvestri, V.; Schipper, K.; Cohen, J.D.; Fairchild, A.N.; Gorin, M.A.; Verdone, J.E.; Pienta, K.J.; Bader, J.S.; et al.et al Polyclonal breast cancer metastases arise from collective dissemination of keratin 14-expressing tumor cell clusters. Proc. Natl. Acad. Sci. USA 2016, 113, E854-E863.
  70. Nicola Aceto; Mehmet Toner; Shyamala Maheswaran; Daniel A. Haber; En Route to Metastasis: Circulating Tumor Cell Clusters and Epithelial-to-Mesenchymal Transition. Trends in Cancer 2015, 1, 44-52, 10.1016/j.trecan.2015.07.006.
  71. Gkountela, S.; Castro-Giner, F.; Szczerba, B.M.; Vetter, M.; Landin, J.; Scherrer, R.; Krol, I.; Scheidmann, M.C.; Beisel, C.; Stirnimann, C.U.; et al.et al Circulating Tumor Cell Clustering Shapes DNA Methylation to Enable Metastasis Seeding. Cell 2019, 176, 98-112.e14, 10.1016/j.cell.2018.11.046.
  72. Liu, X.; Taftaf, R.; Kawaguchi, M.; Chang, Y.F.; Chen, W.; Entenberg, D.; Zhang, Y.; Gerratana, L.; Huang, S.; Patel, D.B.; et al.et al Homophilic CD44 Interactions Mediate Tumor Cell Aggregation and Polyclonal Metastasis in Patient-Derived Breast Cancer Models. Cancer Discov. 2019, 9, 96-113, 10.1158/2159-8290.cd-18-0065.
  73. Giuliano, M.; Shaikh, A.; Lo, H.C.; Arpino, G.; De Placido, S.; Zhang, X.H.; Cristofanilli, M.; Schiff, R.; Trivedi, M.V; Perspective on Circulating Tumor Cell Clusters: Why It Takes a Village to Metastasize. Cancer Research 2018, 78, 845-852, 10.1158/0008-5472.can-17-2748.
  74. Zhao, Q.; Barclay, M.; Hilkens, J.; Guo, X.; Barrow, H.; Rhodes, J.M.; Yu, L.G; Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumour cell homotypic aggregation and prevents anoikis. Molecular Cancer 2010, 9, 154, 10.1186/1476-4598-9-154.
  75. Sharma, D.; Brummel-Ziedins, K.E.; Bouchard, B.A.; Holmes, C.E; Platelets in Tumor Progression: A Host Factor That Offers Multiple Potential Targets in the Treatment of Cancer. Journal of Cellular Physiology 2014, 229, 1005-1015, 10.1002/jcp.24539.
  76. Duda, D.G.; Duyverman, A.M.; Kohno, M.; Snuderl, M.; Steller, E.J.; Fukumura, D.; Jain, R.K; Malignant cells facilitate lung metastasis by bringing their own soil.. Proceedings of the National Academy of Sciences 2010, 107, 21677-82, 10.1073/pnas.1016234107.
  77. Au, S.H.; Storey, B.D.; Moore, J.C.; Tang, Q.; Chen, Y.L.; Javaid, S.; Sarioglu, A.F.; Sullivan, R.; Madden, M.W.; O’Keefe, R; et al. Clusters of circulating tumor cells traverse capillary-sized vessels.. Proceedings of the National Academy of Sciences 2016, 113, 4947-4952, 10.1073/pnas.1524448113.
  78. Thery, L.; Meddis, A.; Cabel, L.; Proudhon, C.; Latouche, A.; Pierga, J.Y.; Bidard, F.C; Circulating Tumor Cells in Early Breast Cancer. JNCI Cancer Spectr. 2019, 3, pkz026.
  79. Bidard, F.C.; Michiels, S.; Riethdorf, S.; Mueller, V.; Esserman, L.J.; Lucci, A.; Naume, B.; Horiguchi, J.; Gisbert-Criado, R.; Sleijfer, S; et al. Circulating Tumor Cells in Breast Cancer Patients Treated by Neoadjuvant Chemotherapy: A Meta-analysis. JNCI: Journal of the National Cancer Institute 2018, 110, 560-567, 10.1093/jnci/djy018.
  80. Lucci, A.; Hall, C.S.; Lodhi, A.K.; Bhattacharyya, A.; Anderson, A.E.; Xiao, L.; Bedrosian, I.; Kuerer, H.M.; Krishnamurthy, S; Circulating tumour cells in non-metastatic breast cancer: a prospective study. The Lancet Oncology 2012, 13, 688-695, 10.1016/s1470-2045(12)70209-7.
  81. Rack, B.; Schindlbeck, C.; Juckstock, J.; Andergassen, U.; Hepp, P.; Zwingers, T.; Friedl, T.W.; Lorenz, R.; Tesch, H.; Fasching, P.A; et al. Circulating tumor cells predict survival in early average-to-high risk breast cancer patients.. JNCI: Journal of the National Cancer Institute 2014, 106, none.
  82. Janni, W.J.; Rack, B.; Terstappen, L.W.; Pierga, J.Y.; Taran, F.A.; Fehm, T.; Hall, C.; de Groot, M.R.; Bidard, F.C.; Friedl, T.W; et al. Pooled Analysis of the Prognostic Relevance of Circulating Tumor Cells in Primary Breast Cancer. Clinical Cancer Research 2016, 22, 2583-2593, 10.1158/1078-0432.ccr-15-1603.
  83. Ignatiadis, M.; Rothe, F.; Chaboteaux, C.; Durbecq, V.; Rouas, G.; Criscitiello, C.; Metallo, J.; Kheddoumi, N.; Singhal, S.K.; Michiels, S.; et al. HER2-positive circulating tumor cells in breast cancer. PLoS ONE 2011, 6, e15624.
  84. Sparano, J.; O’Neill, A.; Alpaugh, K.; Wolff, A.C.; Northfelt, D.W.; Dang, C.T.; Sledge, G.W.; Miller, K.D; Association of Circulating Tumor Cells With Late Recurrence of Estrogen Receptor-Positive Breast Cancer: A Secondary Analysis of a Randomized Clinical Trial.. JAMA Oncology 2018, 4, 1700-1706, 10.1001/jamaoncol.2018.2574.
  85. Janni, W.; Rack, B.K.; Fasching, P.A.; Haeberle, L.; Tesch, H.; Lorenz, R.; Schochter, F.; Tzschaschel, M.; Gregorio, A.D.; Fehm, T.N.; et al. Persistence of circulating tumor cells in high risk early breast cancer patients five years after adjuvant chemotherapy and late recurrence: Results from the adjuvant SUCCESS A trial. J. Clin. Oncol. 2018, 36, 515.
  86. Trapp, E.; Janni, W.; Schindlbeck, C.; Juckstock, J.; Andergassen, U.; de Gregorio, A.; Alunni-Fabbroni, M.; Tzschaschel, M.; Polasik, A.; Koch, J.G; et al. Presence of Circulating Tumor Cells in High-Risk Early Breast Cancer During Follow-Up and Prognosis. JNCI: Journal of the National Cancer Institute 2019, 111, 380-387, 10.1093/jnci/djy152.
  87. Goodman, C.R.; Seagle, B.L.; Friedl, T.W.P.; Rack, B.; Lato, K.; Fink, V.; Cristofanilli, M.; Donnelly, E.D.; Janni, W.; Shahabi, S; et al. Association of Circulating Tumor Cell Status With Benefit of Radiotherapy and Survival in Early-Stage Breast Cancer.. JAMA Oncology 2018, 4, e180163, 10.1001/jamaoncol.2018.0163.
  88. Ignatiadis, M.; Litiere, S.; Rothe, F.; Riethdorf, S.; Proudhon, C.; Fehm, T.; Aalders, K.; Forstbauer, H.; Fasching, P.A.; Brain, E.; et al. Trastuzumab versus observation for HER2 nonamplified early breast cancer with circulating tumor cells (EORTC 90091-10093, BIG 1-12, Treat CTC): A randomized phase II trial. Ann. Oncol. 2018, 29, 1777–1783.
  89. Zhang, L.; Riethdorf, S.; Wu, G.; Wang, T.; Yang, K.; Peng, G.; Liu, J.; Pantel, K; Meta-Analysis of the Prognostic Value of Circulating Tumor Cells in Breast Cancer. Clinical Cancer Research 2012, 18, 5701-5710, 10.1158/1078-0432.ccr-12-1587.
  90. Giordano, A.; Giuliano, M.; Hsu, L.; Handy, B.C.; Ueno, N.T.; Andreopoulou, E.; Alvarez, R.H.; Valero, V.; Hortobagyi, G.N.; Cristofanilli, M; et al. Prognostic value of circulating tumor cells (CTC) in metastatic breast cancer (MBC): Correlation with immunohistochemically defined molecular subtypes and metastatic disease sites. J. Clin. Oncol. 2010, 28, 1000.
  91. Budd, G.T.; Cristofanilli, M.; Ellis, M.J.; Stopeck, A.; Borden, E.; Miller, M.C.; Matera, J.; Repollet, M.; Doyle, G.V.; Terstappen, L.W; et al. irculating tumor cells versus imaging--predicting overall survival in metastatic breast cancer. Clin. Cancer Res. 2006, 12, 6403–6409, 10.1186/s13058-019-1215-z.
  92. Cristofanilli, M.; Budd, G.T.; Ellis, M.J.; Stopeck, A.; Matera, J.; Miller, M.C.; Reuben, J.M.; Doyle, G.V.; Allard, W.J.; Terstappen, L.W; et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 2004, 351, 781–791.
  93. Banys-Paluchowski, M.; Fehm, T.; Janni, W.; Solomayer, E.F.; Hartkopf, A; Circulating and Disseminated Tumor Cells in Breast Carcinoma: Report from the Consensus Conference on Tumor Cell Dissemination during the 39th Annual Meeting of the German Society of Senology, Berlin, 27 June 2019. Geburtshilfe Frauenheilkd 2019, 79, 1320–1327.
  94. Cristofanilli, M.; Pierga, J.Y.; Reuben, J.; Rademaker, A.; Davis, A.A.; Peeters, D.J.; Fehm, T.; Nole, F.; Gisbert-Criado, R.; Mavroudis, D.; et al.et al. Bidard, F.-C.; Jacot, W.; Dureau, S.; Brain, E.; Bachelot, T.; Bourgeois, H.; Goncalves, A.; Ladoire, S.; Naman, H.; Dalenc, F. Cancer Res. 2019, 79, GS3-07-GS03-07.
  95. Smerage, J.B.; Barlow, W.E.; Hortobagyi, G.N.; Winer, E.P.; Leyland-Jones, B.; Srkalovic, G.; Tejwani, S.; Schott, A.F.; O’Rourke, M.A.; Lew, D.L; et al. Circulating Tumor Cells and Response to Chemotherapy in Metastatic Breast Cancer: SWOG S0500. Journal of Clinical Oncology 2014, 32, 3483-3489, 10.1200/jco.2014.56.2561.
  96. Jacot, W.; Cottu, P.; Berger, F.; Dubot, C.; Venat-Bouvet, L.; Lortholary, A.; Bourgeois, H.; Bollet, M.; Servent, V.; Luporsi, E; et al. Actionability of HER2-amplified circulating tumor cells in HER2-negative metastatic breast cancer: the CirCe T-DM1 trial.. Breast Cancer Research 2019, 21, 121, 10.1186/s13058-019-1215-z.
  97. Polasik, A.; Schramm, A.; Friedl, T.W.P.; Rack, B.K.; Trapp, E.K.; Fasching, P.A.; Taran, F.-A.; Hartkopf, A.D.; Schneeweiss, A.; Mueller, V; et al. The DETECT study concept: Individualized therapy of metastatic breast cancer. Journal of Clinical Oncology 2016, 34, TPS634.
  98. Paoletti, C.; Miao, J.; Dolce, E.M.; Darga, E.P.; Repollet, M.I.; Doyle, G.V.; Gralow, J.R.; Hortobagyi, G.N.; Smerage, J.B.; Barlow, W.E; et al. Circulating Tumor Cell Clusters in Patients with Metastatic Breast Cancer: a SWOG S0500 Translational Medicine Study. Clinical Cancer Research 2019, 25, 6089-6097, 10.1158/1078-0432.CCR-19-0208.
  99. Cristofanilli, M.; Pierga, J.Y.; Reuben, J.; Rademaker, A.; Davis, A.A.; Peeters, D.J.; Fehm, T.; Nole, F.; Gisbert-Criado, R.; Mavroudis, D; et al. The clinical use of circulating tumor cells (CTCs) enumeration for staging of metastatic breast cancer (MBC): International expert consensus paper. Crit. Rev. Oncol. Hematol. 2019, 134, 39–45.
  100. Schochter, F.; Friedl, T.W.P.; deGregorio, A.; Krause, S.; Huober, J.; Rack, B.; Janni, W; Are Circulating Tumor Cells (CTCs) Ready for Clinical Use in Breast Cancer? An Overview of Completed and Ongoing Trials Using CTCs for Clinical Treatment Decisions. Cell 2019, 8, 1412.
  101. Bidard, F.C.; Fehm, T.; Ignatiadis, M.; Smerage, J.B.; Alix-Panabieres, C.; Janni, W.; Messina, C.; Paoletti, C.; Muller, V.; Hayes, D.F; et al. Clinical application of circulating tumor cells in breast cancer: overview of the current interventional trials.. Cancer and Metastasis Reviews 2013, 32, 179-88, 10.1007/s10555-012-9398-0.
  102. Gabriel, M.T.; Calleja, L.R.; Chalopin, A.; Ory, B.; Heymann, D; Circulating Tumor Cells: A Review of Non–EpCAM-Based Approaches for Cell Enrichment and Isolation. Clinical Chemistry 2016, 62, 571-581, 10.1373/clinchem.2015.249706.
  103. Agerbaek MO, Bang-Christensen SR, Yang MH, Clausen TM, Pereira MA, Sharma S; The VAR2CSA malaria protein efficiently retrieves circulating tumor cells in an EpCAM-independent manner.. Nature Communications 2018, 9, 3279, 10.1038/s41467-018-05793-2.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Feedback