Going with the flow: From circulating tumor cells to DNA

Science Translational Medicine

Volumn 5, Issue 207, 2013, Pages

  Bidard, Francois Clement ^a,b   Weigelt, Britta ^a   Reis Filho, Jorge S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULATING TUMOR DNA; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; LAPATINIB; PERTUZUMAB; TRASTUZUMAB; TUMOR MARKER; UNCLASSIFIED DRUG;

BREAST CANCER; BREAST METASTASIS; CANCER CELL; CANCER DIAGNOSIS; CIRCULATING TUMOR CELL; DISEASE MARKER; DNA DETERMINATION; EARLY DIAGNOSIS; GENE AMPLIFICATION; GENE FREQUENCY; GENE MUTATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HUMAN; LUNG NON SMALL CELL CANCER; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS;

DNA, NEOPLASM; HUMANS; NEOPLASTIC CELLS, CIRCULATING; POINT MUTATION; TUMOR MARKERS, BIOLOGICAL;

EID: 84886379960     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006305     Document Type: Review

References (57)

1. L. A. Garraway, E. S. Lander, Lessons from the cancer genome. Cell 153, 17-37 (2013).
2. M. Gerlinger, A. J. Rowan, S. Horswell, J. Larkin, D. Endesfelder, E. Gronroos, P. Martinez, N. Matthews, A. Stewart, P. Tarpey, I. Varela, B. Phillimore, S. Begum, N. Q. McDonald, A. Butler, D. Jones, K. Raine, C. Latimer, C. R. Santos, M. Nohadani, A. C. Eklund, B. Spencer-Dene, G. Clark, L. Pickering, G. Stamp, M. Gore, Z. Szallasi, J. Downward, P. A. Futreal, C. Swanton, Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892 (2012).
3. N. Navin, J. Kendall, J. Troge, P. Andrews, L. Rodgers, J. McIndoo, K. Cook, A. Stepansky, D. Levy, D. Esposito, L. Muthuswamy, A. Krasnitz, W. R. McCombie, J. Hicks, M. Wigler, Tumour evolution inferred by single-cell sequencing. Nature 472, 90-94 (2011).
4. S. Nik-Zainal, P. Van Loo, D. C. Wedge, L. B. Alexandrov, C. D. Greenman, K. W. Lau, K. Raine, D. Jones, J. Marshall, M. Ramakrishna, A. Shlien, S. L. Cooke, J. Hinton, A. Menzies, L. A. Stebbings, C. Leroy, M. Jia, R. Rance, L. J. Mudie, S. J. Gamble, P. J. Stephens, S. McLaren, P. S. Tarpey, E. Papaemmanuil, H. R. Davies, I. Varela, D. J. McBride, G. R. Bignell, K. Leung, A. P. Butler, J. W. Teague, S. Martin, G. Jönsson, O. Mariani, S. Boyault, P. Miron, A. Fatima, A. Langerød, S. A. Aparicio, A. Tutt, A. M. Sieuwerts, A. Borg, G. Thomas, A. V. Salomon, A. L. Richardson, A. L. Børresen-Dale, P. A. Futreal, M. R. Stratton, P. J. CampbellBreast Cancer Working Group of the International Cancer Genome Consortium, The life history of 21 breast cancers. Cell 149, 994-1007 (2012).
5. S. P. Shah, A. Roth, R. Goya, A. Oloumi, G. Ha, Y. Zhao, G. Turashvili, J. Ding, K. Tse, G. Haffari, A. Bashashati, L. M. Prentice, J. Khattra, A. Burleigh, D. Yap, V. Bernard, A. McPherson, K. Shumansky, A. Crisan, R. Giuliany, A. Heravi-Moussavi, J. Rosner, D. Lai, I. Birol, R. Varhol, A. Tam, N. Dhalla, T. Zeng, K. Ma, S. K. Chan, M. Griffith, A. Moradian, S. W. Cheng, G. B. Morin, P. Watson, K. Gelmon, S. Chia, S. F. Chin, C. Curtis, O. M. Rueda, P. D. Pharoah, S. Damaraju, J. Mackey, K. Hoon, T. Harkins, V. Tadigotla, M. Sigaroudinia, P. Gascard, T. Tlsty, J. F. Costello, I. M. Meyer, C. J. Eaves, W. W. Wasserman, S. Jones, D. Huntsman, M. Hirst, C. Caldas, M. A. Marra, S. Aparicio, The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 486, 395-399 (2012).
6. L. Ding, M. J. Ellis, S. Li, D. E. Larson, K. Chen, J. W. Wallis, C. C. Harris, M. D. McLellan, R. S. Fulton, L. L. Fulton, R. M. Abbott, J. Hoog, D. J. Dooling, D. C. Koboldt, H. Schmidt, J. Kalicki, Q. Zhang, L. Chen, L. Lin, M. C. Wendl, J. F. McMichael, V. J. Magrini, L. Cook, S. D. McGrath, T. L. Vickery, E. Appelbaum, K. Deschryver, S. Davies, T. Guintoli, L. Lin, R. Crowder, Y. Tao, J. E. Snider, S. M. Smith, A. F. Dukes, G. E. Sanderson, C. S. Pohl, K. D. Delehaunty, C. C. Fronick, K. A. Pape, J. S. Reed, J. S. Robinson, J. S. Hodges, W. Schierding, N. D. Dees, D. Shen, D. P. Locke, M. E. Wiechert, J. M. Eldred, J. B. Peck, B. J. Oberkfell, J. T. Lolofie, F. Du, A. E. Hawkins, M. D. O'Laughlin, K. E. Bernard, M. Cunningham, G. Elliott, M. D. Mason, D. M. Thompson Jr., J. L. Ivanovich, P. J. Goodfellow, C. M. Perou, G. M. Weinstock, R. Aft, M. Watson, T. J. Ley, R. K. Wilson, E. R. Mardis, Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 464, 999-1005 (2010).
7. S. P. Shah, R. D. Morin, J. Khattra, L. Prentice, T. Pugh, A. Burleigh, A. Delaney, K. Gelmon, R. Guliany, J. Senz, C. Steidl, R. A. Holt, S. Jones, M. Sun, G. Leung, R. Moore, T. Severson, G. A. Taylor, A. E. Teschendorff, K. Tse, G. Turashvili, R. Varhol, R. L. Warren, P. Watson, Y. Zhao, C. Caldas, D. Huntsman, M. Hirst, M. A. Marra, S. Aparicio, Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461, 809-813 (2009).
8. P. L. Bedard, A. R. Hansen, M. J. Ratain, L. L. Siu, Tumour heterogeneity in the clinic. Nature 501, 355-364 (2013).
9. R. A. Burrell, N. McGranahan, J. Bartek, C. Swanton, The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338-345 (2013).
10. J. Y. Pierga, D. Hajage, T. Bachelot, S. Delaloge, E. Brain, M. Campone, V. Diéras, E. Rolland, L. Mignot, C. Mathiot, F. C. Bidard, High independent prognostic and predictive value of circulating tumor cells compared with serum tumor markers in a large prospective trial in first-line chemotherapy for metastatic breast cancer patients. Ann. Oncol. 23, 618-624 (2012).
11. S. J. Dawson, D. W. Tsui, M. Murtaza, H. Biggs, O. M. Rueda, S. F. Chin, M. J. Dunning, D. Gale, T. Forshew, B. Mahler-Araujo, S. Rajan, S. Humphray, J. Becq, D. Halsall, M. Wallis, D. Bentley, C. Caldas, N. Rosenfeld, Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl. J. Med. 368, 1199-1209 (2013).
12. K. C. Chan, P. Jiang, Y. W. Zheng, G. J. Liao, H. Sun, J. Wong, S. S. Siu, W. C. Chan, S. L. Chan, A. T. Chan, P. B. Lai, R. W. Chiu, Y. M. Lo, Cancer genome scanning in plasma: detection of tumor-associated copy number aberrations, single-nucleotide variants, and tumoral heterogeneity by massively parallel sequencing. Clin. Chem. 59, 211-224 (2013).
13. T. Forshew, M. Murtaza, C. Parkinson, D. Gale, D. W. Y. Tsui, F. Kaper, S. J. Dawson, A. M. Piskorz, M. Jimenez-Linan, D. Bentley, J. Hadfield, A. P. May, C. Caldas, J. D. Brenton, N. Rosenfeld, Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci. Transl. Med. 4, 136ra68 (2012).
14. R. J. Leary, M. Sausen, I. Kinde, N. Papadopoulos, J. D. Carpten, D. Craig, J. O'Shaughnessy, K. W. Kinzler, G. Parmigiani, B. Vogelstein, L. A. Diaz Jr., V. E. Velculescu, Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing. Sci. Transl. Med. 4, 162ra154 (2012).
15. M. Murtaza, S. J. Dawson, D. W. Tsui, D. Gale, T. Forshew, A. M. Piskorz, C. Parkinson, S. F. Chin, Z. Kingsbury, A. S. Wong, F. Marass, S. Humphray, J. Hadfield, D. Bentley, T. M. Chin, J. D. Brenton, C. Caldas, N. Rosenfeld, Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 497, 108-112 (2013).
16. N. C. Turner, J. S. Reis-Filho, Genetic heterogeneity and cancer drug resistance. Lancet Oncol. 13, e178-e185 (2012).
17. C. Alix-Panabières, K. Pantel, Circulating tumor cells: Liquid biopsy of cancer. Clin. Chem. 59, 110-118 (2013).
18. J. M. Lang, B. P. Casavant, D. J. Beebe, Circulating tumor cells: Getting more from less. Sci. Transl. Med. 4, 141ps13 (2012).
19. D. R. Parkinson, N. Dracopoli, B. G. Petty, C. Compton, M. Cristofanilli, A. Deisseroth, D. F. Hayes, G. Kapke, P. Kumar, J. Sh. Lee, M. C. Liu, R. McCormack, S. Mikulski, L. Nagahara, K. Pantel, S. Pearson-White, E. A. Punnoose, L. T. Roadcap, A. E. Schade, H. I. Scher, C. C. Sigman, G. J. Kelloff, Considerations in the development of circulating tumor cell technology for clinical use. J. Transl. Med. 10, 138 (2012).
20. M. Yu, S. Stott, M. Toner, S. Maheswaran, D. A. Haber, Circulating tumor cells: Approaches to isolation and characterization. J. Cell Biol. 192, 373-382 (2011).
21. M. S. Wicha, D. F. Hayes, Circulating tumor cells: Not all detected cells are bad and not all bad cells are detected. J. Clin. Oncol. 29, 1508-1511 (2011).
22. H. Schwarzenbach, C. Alix-Panabières, I. Müller, N. Letang, J. P. Vendrell, X. Rebillard, K. Pantel, Cell-free tumor DNA in blood plasma as a marker for circulating tumor cells in prostate cancer. Clin. Cancer Res. 15, 1032-1038 (2009).
23. F. Diehl, M. Li, D. Dressman, Y. He, D. Shen, S. Szabo, L. A. Diaz Jr., S. N. Goodman, K. A. David, H. Juhl, K. W. Kinzler, B. Vogelstein, Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc. Natl. Acad. Sci. U.S.A. 102, 16368-16373 (2005).
24. R. E. Board, A. M. Wardley, J. M. Dixon, A. C. Armstrong, S. Howell, L. Renshaw, E. Donald, A. Greystoke, M. Ranson, A. Hughes, C. Dive, Detection of PIK3CA mutations in circulating free DNA in patients with breast cancer. Breast Cancer Res. Treat. 120, 461-467 (2010).
25. J. Däbritz, J. Hänfler, R. Preston, J. Stieler, H. Oettle, Detection of Ki-ras mutations in tissue and plasma samples of patients with pancreatic cancer using PNA-mediated PCR clamping and hybridisation probes. Br. J. Cancer 92, 405-412 (2005).
26. M. J. Higgins, D. Jelovac, E. Barnathan, B. Blair, S. Slater, P. Powers, J. Zorzi, S. C. Jeter, G. R. Oliver, J. Fetting, L. Emens, C. Riley, V. Stearns, F. Diehl, P. Angenendt, P. Huang, L. Cope, P. Argani, K. M. Murphy, K. E. Bachman, J. Greshock, A. C. Wolff, B. H. Park, Detection of tumor PIK3CA status in metastatic breast cancer using peripheral blood. Clin. Cancer Res. 18, 3462-3469 (2012).
27. J. Madic, S. Piperno-Neumann, V. Servois, A. Rampanou, M. Milder, B. Trouiller, D. Gentien, S. Saada, F. Assayag, A. Thuleau, F. Nemati, D. Decaudin, F. C. Bidard, L. Desjardins, P. Mariani, O. Lantz, M. H. Stern, Pyrophosphorolysis-activated polymerization detects circulating tumor DNA in metastatic uveal melanoma. Clin. Cancer Res. 18, 3934-3941 (2012).
28. L. Benesova, B. Belsanova, S. Suchanek, M. Kopeckova, P. Minarikova, L. Lipska, M. Levy, V. Visokai, M. Zavoral, M. Minarik, Mutation-based detection and monitoring of cell-free tumor DNA in peripheral blood of cancer patients. Anal. Biochem. 433, 227-234 (2013).
29. R. J. Leary, I. Kinde, F. Diehl, K. Schmidt, C. Clouser, C. Duncan, A. Antipova, C. Lee, K. McKernan, F. M. De La Vega, K. W. Kinzler, B. Vogelstein, L. A. Diaz Jr., V. E. Velculescu, Development of personalized tumor biomarkers using massively parallel sequencing. Sci. Transl. Med. 2, 20ra14 (2010).
30. Z. Chen, J. Feng, C. H. Buzin, Q. Liu, L. Weiss, K. Kernstine, G. Somlo, S. S. Sommer, Analysis of cancer mutation signatures in blood by a novel ultra-sensitive assay: monitoring of therapy or recurrence in non-metastatic breast cancer. PLOS ONE 4, e7220 (2009).
31. M. Gundry, J. Vijg, Direct mutation analysis by high-throughput sequencing: From germline to low-abundant, somatic variants. Mutat. Res. 729, 1-15 (2012).
32. E. Heitzer, P. Ulz, J. Belic, S. Gutschi, F. Quehenberger, K. Fischereder, T. Benezeder, M. Auer, C. Pischler, S. Mannweiler, M. Pichler, F. Eisner, M. Haeusler, S. Riethdorf, K. Pantel, H. Samonigg, G. Hoefler, H. Augustin, J. B. Geigl, M. R. Speicher, Tumor-associated copy number changes in the circulation of patients with prostate cancer identified through whole-genome sequencing. Genome Med. 5, 30 (2013).
33. I. Kinde, J. Wu, N. Papadopoulos, K. W. Kinzler, B. Vogelstein, Detection and quantification of rare mutations with massively parallel sequencing. Proc. Natl. Acad. Sci. U.S.A. 108, 9530-9535 (2011).
34. A. Narayan, N. J. Carriero, S. N. Gettinger, J. Kluytenaar, K. R. Kozak, T. I. Yock, N. E. Muscato, P. Ugarelli, R. H. Decker, A. A. Patel, Ultrasensitive measurement of hotspot mutations in tumor DNA in blood using error-suppressed multiplexed deep sequencing. Cancer Res. 72, 3492-3498 (2012).
35. M. W. Schmitt, S. R. Kennedy, J. J. Salk, E. J. Fox, J. B. Hiatt, L. A. Loeb, Detection of ultra-rare mutations by next-generation sequencing. Proc. Natl. Acad. Sci. U.S.A. 109, 14508-14513 (2012).
36. F. Mouliere, A. R. Thierry, The importance of examining the proportion of circulating DNA originating from tumor, microenvironment and normal cells in colorectal cancer patients. Expert Opin. Biol. Ther. 12, S209-S215 (2012).
37. H. Schwarzenbach, D. S. Hoon, K. Pantel, Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 11, 426-437 (2011).
38. V. Müller, D. F. Hayes, K. Pantel, Recent translational research: circulating tumor cells in breast cancer patients. Breast Cancer Res. 8, 110 (2006).
39. S. T. Ligthart, F. C. Bidard, C. Decraene, T. Bachelot, S. Delaloge, E. Brain, M. Campone, P. Viens, J. Y. Pierga, L. W. Terstappen, Unbiased quantitative assessment of Her-2 expression of circulating tumor cells in patients with metastatic and non-metastatic breast cancer. Ann. Oncol. 24, 1231-1238 (2013).
40. R. Nadal, A. Fernandez, P. Sanchez-Rovira, M. Salido, M. Rodríguez, J. L. García-Puche, M. Macià, J. M. Corominas, M. Delgado-Rodriguez, L. Gonzalez, J. Albanell, M. Fernández, F. Solé, J. A. Lorente, M. J. Serrano, Biomarkers characterization of circulating tumour cells in breast cancer patients. Breast Cancer Res. 14, R71 (2012).
41. G. Somlo, S. K. Lau, P. Frankel, H. B. Hsieh, X. Liu, L. Yang, R. Krivacic, R. H. Bruce, Multiple biomarker expression on circulating tumor cells in comparison to tumor tissues from primary and metastatic sites in patients with locally advanced/inflammatory, and stage IV breast cancer, using a novel detection technology. Breast Cancer Res. Treat. 128, 155-163 (2011).
42. E. Heitzer, M. Auer, C. Gasch, M. Pichler, P. Ulz, E. M. Hoffmann, S. Lax, J. Waldispuehl-Geigl, O. Mauermann, C. Lackner, G. Höfler, F. Eisner, H. Sill, H. Samonigg, K. Pantel, S. Riethdorf, T. Bauernhofer, J. B. Geigl, M. R. Speicher, Complex tumor genomes inferred from single circulating tumor cells by array-CGH and next-generation sequencing. Cancer Res. 73, 2965-2975 (2013).
43. C. Gasch, T. Bauernhofer, M. Pichler, S. Langer-Freitag, M. Reeh, A. M. Seifert, O. Mauermann, J. R. Izbicki, K. Pantel, S. Riethdorf, Heterogeneity of epidermal growth factor receptor status and mutations of KRAS/PIK3CA in circulating tumor cells of patients with colorectal cancer. Clin. Chem. 59, 252-260 (2013).
44. S. Aparicio, C. Caldas, The implications of clonal genome evolution for cancer medicine. N. Engl. J. Med. 368, 842-851 (2013).
45. N. Niikura, J. Liu, N. Hayashi, E. A. Mittendorf, Y. Gong, S. L. Palla, Y. Tokuda, A. M. Gonzalez-Angulo, G. N. Hortobagyi, N. T. Ueno, Loss of human epidermal growth factor receptor 2 (HER2) expression in metastatic sites of HER2-overexpressing primary breast tumors. J. Clin. Oncol. 30, 593-599 (2012).
46. H. Gevensleben, I. Garcia-Murillas, M. K. Graeser, G. Schiavon, P. Osin, M. Parton, I. E. Smith, A. Ashworth, N. C. Turner, Noninvasive detection of HER2 amplification with plasma DNA digital PCR. Clin. Cancer Res. 19, 3276-3284 (2013).
47. M. Yu, A. Bardia, B. S. Wittner, S. L. Stott, M. E. Smas, D. T. Ting, S. J. Isakoff, J. C. Ciciliano, M. N. Wells, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, S. Maheswaran, Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580-584 (2013).
48. S. Maheswaran, L. V. Sequist, S. Nagrath, L. Ulkus, B. Brannigan, C. V. Collura, E. Inserra, S. Diederichs, A. J. Iafrate, D. W. Bell, S. Digumarthy, A. Muzikansky, D. Irimia, J. Settleman, R. G. Tompkins, T. J. Lynch, M. Toner, D. A. Haber, Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med. 359, 366-377 (2008).
49. L. A. Diaz Jr., R. T. Williams, J. Wu, I. Kinde, J. R. Hecht, J. Berlin, B. Allen, I. Bozic, J. G. Reiter, M. A. Nowak, K. W. Kinzler, K. S. Oliner, B. Vogelstein, The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486, 537-540 (2012).
50. C. A. Klein, Selection and adaptation during metastatic cancer progression. Nature 501, 365-372 (2013).
51. A. Marusyk, K. Polyak, Tumor heterogeneity: Causes and consequences. Biochim. Biophys. Acta 1805, 105-117 (2010).
52. J. B. Hiatt, C. C. Pritchard, S. J. Salipante, B. J. O'Roak, J. Shendure, Single molecule molecular inversion probes for targeted, high-accuracy detection of low-frequency variation. Genome Res. 23, 843-854 (2013).
53. F. C. Bidard, T. Fehm, M. Ignatiadis, J. B. Smerage, C. Alix-Panabières, W. Janni, C. Messina, C. Paoletti, V. Müller, D. F. Hayes, M. Piccart, J. Y. Pierga, Clinical application of circulating tumor cells in breast cancer: Overview of the current interventional trials. Cancer Metastasis Rev. 32, 179-188 (2013).
54. E. A. Punnoose, S. Atwal, W. Liu, R. Raja, B. M. Fine, B. G. Hughes, R. J. Hicks, G. M. Hampton, L. C. Amler, A. Pirzkall, M. R. Lackner, Evaluation of circulating tumor cells and circulating tumor DNA in non-small cell lung cancer: association with clinical endpoints in a phase II clinical trial of pertuzumab and erlotinib. Clin. Cancer Res. 18, 2391-2401 (2012).
55. I. Van der Auwera, H. J. Elst, S. J. Van Laere, H. Maes, P. Huget, P. van Dam, E. A. Van Marck, P. B. Vermeulen, L. Y. Dirix, The presence of circulating total DNA and methylated genes is associated with circulating tumour cells in blood from breast cancer patients. Br. J. Cancer 100, 1277-1286 (2009).
56. M. Chimonidou, A. Strati, N. Malamos, V. Georgoulias, E. S. Lianidou, SOX17 promoter methylation in circulating tumor cells and matched cell-free DNA isolated from plasma of patients with breast cancer. Clin. Chem. 59, 270-279 (2013).
57. F. C. Bidard, J. Madic, P. Mariani, S. Piperno-Neumann, A. Rampanou, V. Servois, N. Cassoux, L. Desjardins, M. Milder, I. Vaucher, J. Y. Pierga, R. Lebofsky, M. H. Stern, O. Lantz, Detection rate and prognostic value of circulating tumor cells and circulating tumor DNA in metastatic uveal melanoma. Int. J. Cancer (12 August 2013) 10.1002/ijc.28436.