Circulating tumor cells and circulating tumor DNA for precision medicine: Dream or reality?

Annals of Oncology

Volumn 25, Issue 12, 2014, Pages 2304-2313

  Ignatiadis, Michail ^a   Dawson, S J ^b  

^a JULES BORDET INSTITUTE   (Belgium)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Circulating tumor cells; Circulating tumor DNA; Liquid biopsy; Precision medicine

Indexed keywords

CIRCULATING TUMOR DNA; DNA; UNCLASSIFIED DRUG;

CANCER PATIENT; CIRCULATING TUMOR CELL; CLINICAL PRACTICE; EVOLUTION; HUMAN; MEDICAL DECISION MAKING; METASTASIS; MONITORING; NEOPLASM; NEXT GENERATION SEQUENCING; NONHUMAN; OUTCOME ASSESSMENT; PRECISION MEDICINE; PRIMARY TUMOR; PRIORITY JOURNAL; REVIEW; THERAPY; TREATMENT FAILURE; BLOOD; GENETICS; HIGH THROUGHPUT SEQUENCING; NEOPLASMS; TUMOR EMBOLISM;

DNA, NEOPLASM; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING;

EID: 84926459432     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdu480     Document Type: Review

References (116)

1. Yates LR, Campbell PJ. Evolution of the cancer genome. Nat Rev Genet 2012; 13: 795-806.
2. Aparicio S, Caldas C. The implications of clonal genome evolution for cancer medicine. N Engl J Med 2013; 368: 842-851.
3. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011; 147: 275-292.
4. Nik-Zainal S, Van Loo P, Wedge DC et al. The life history of 21 breast cancers. Cell 2012; 149: 994-1007.
5. Gerlinger M, Rowan AJ, Horswell S et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012; 366: 883-892.
6. Ignatiadis M, Sotiriou C. Luminal breast cancer: from biology to treatment. Nat Rev Clin Oncol 2013; 10: 494-506.
7. Aguirre-Ghiso JA. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 2007; 7: 834-846.
8. Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer 2009; 9: 302-312.
9. Ashworth T. A case of cancer in which cells similar to those in the tumors were seen in the blood after death. Aust Med J 1869; 14: 146-149.
10. Pantel K, Brakenhoff RH, Brandt B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 2008; 8: 329-340.
11. Alix-Panabieres C, Pantel K. Circulating tumor cells: liquid biopsy of cancer. Clin Chem 2013; 59: 110-118.
12. Miyamoto DT, Sequist LV, Lee RJ. Circulating tumour cells-monitoring treatment response in prostate cancer. Nat Rev Clin Oncol 2014; 11: 401-412.
13. Lianidou ES. Circulating tumor cells-new challenges ahead. Clin Chem 2012; 58: 805-807.
14. Sieuwerts AM, Kraan J, Bolt J et al. Anti-epithelial cell adhesion molecule antibodies and the detection of circulating normal-like breast tumor cells. J Natl Cancer Inst 2009; 101: 61-66.
15. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
16. Yu M, Bardia A, Wittner BS et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013; 339: 580-584.
17. Balasubramanian P, Lang JC, Jatana KR et al. Multiparameter analysis, including EMT markers, on negatively enriched blood samples from patients with squamous cell carcinoma of the head and neck. PLoS One 2012; 7: e42048.
18. Karabacak NM, Spuhler PS, Fachin F et al. Microfluidic, marker-free isolation of circulating tumor cells from blood samples. Nat Protoc 2014; 9: 694-710.
19. Lecharpentier A, Vielh P, Perez-Moreno P et al. Detection of circulating tumour cells with a hybrid (epithelial/mesenchymal) phenotype in patients with metastatic non-small cell lung cancer. Br J Cancer 2011; 105: 1338-1341.
20. Kallergi G, Papadaki MA, Politaki E et al. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Res 2011; 13: R59.
21. Coumans FA, Ligthart ST, Uhr JW, Terstappen LW. Challenges in the enumeration and phenotyping of CTC. Clin Cancer Res 2012; 18: 5711-5718.
22. Saucedo-Zeni N, Mewes S, Niestroj R 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: 1241-1250.
23. Ignatiadis M, Reinholz MM. Minimal residual disease and circulating tumor cells in breast cancer. Breast Cancer Res 2011; 13: 222.
24. Parkinson DR, Dracopoli N, Petty BG et al. Considerations in the development of circulating tumor cell technology for clinical use. J Transl Med 2012; 10: 138.
25. Cristofanilli M, Budd GT, Ellis MJ et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 2004; 351: 781-791.
26. de Bono JS, Scher HI, Montgomery RB et al. Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin Cancer Res 2008; 14: 6302-6309.
27. Cohen SJ, Punt CJ, Iannotti N et al. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J Clin Oncol 2008; 26: 3213-3221.
28. Bidard FC, Peeters DJ, Fehm T et al. Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. Lancet Oncol 2014; 15: 406-414.
29. Smerage JB, Barlow WE, Hortobagyi GN et al. Circulating tumor cells and response to chemotherapy in metastatic breast cancer: SWOG S0500. J Clin Oncol 2014 June 2 [epub ahead of print], doi: 10.1200/JCO.2014.56.2561.
30. Scher HI, Heller G, Molina A et al. Evaluation of a composite biomarker panel including circulating tumor cell (CTC) enumeration as a surrogate for survival in metastatic castration-resistant prostate cancer (mCRPC). Eur J Cancer Supp 2013; 11: abstr 2851.
31. Piccart-Gebhart MJ, Procter M, Leyland-Jones B et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 2005; 353: 1659-1672.
32. Prowell TM, Pazdur R. Pathological complete response and accelerated drug approval in early breast cancer. N Engl J Med 2012; 366: 2438-2441.
33. Paik S, Kim C, Wolmark N. HER2 status and benefit from adjuvant trastuzumab in breast cancer. N Engl J Med 2008; 358: 1409-1411.
34. Perez EA, Reinholz MM, Hillman DW et al. HER2 and chromosome 17 effect on patient outcome in the N9831 adjuvant trastuzumab trial. J Clin Oncol 2010; 28: 4307-4315.
35. Ithimakin S, Day KC, Malik F et al. HER2 drives luminal breast cancer stem cells in the absence of HER2 amplification: implications for efficacy of adjuvant trastuzumab. Cancer Res 2013; 73: 1635-1646.
36. Stathopoulou A, Gizi A, Perraki M et al. Real-time quantification of CK-19 mRNApositive cells in peripheral blood of breast cancer patients using the lightcycler system. Clin Cancer Res 2003; 9: 5145-5151.
37. Stathopoulou A, Vlachonikolis I, Mavroudis D et al. Molecular detection of cytokeratin-19-positive cells in the peripheral blood of patients with operable breast cancer: evaluation of their prognostic significance. J Clin Oncol 2002; 20: 3404-3412.
38. Xenidis N, Perraki M, Kafousi M et al. Predictive and prognostic value of peripheral blood cytokeratin-19 mRNA-positive cells detected by real-time polymerase chain reaction in node-negative breast cancer patients. J Clin Oncol 2006; 24: 3756-3762.
39. Ignatiadis M, Xenidis N, Perraki M et al. Different prognostic value of cytokeratin-19 mRNA-positive circulating tumor cells according to estrogen receptor and HER2 status in early breast cancer. J Clin Oncol 2007; 25: 5194-5202.
40. Bozionellou V, Mavroudis D, Perraki M et al. Trastuzumab administration can effectively target chemotherapy-resistant cytokeratin-19 messenger RNA-positive tumor cells in the peripheral blood and bone marrow of patients with breast cancer. Clin Cancer Res 2004; 10: 8185-8194.
41. Georgoulias V, Bozionelou V, Agelaki S et al. Trastuzumab decreases the incidence of clinical relapses in patients with early breast cancer presenting chemotherapy-resistant CK-19mRNA-positive circulating tumor cells: results of a randomized phase II study. Ann Oncol 2012; 23: 1744-1750.
42. Pierga JY, Bidard FC, Mathiot C et al. Circulating tumor cell detection predicts early metastatic relapse after neoadjuvant chemotherapy in large operable and locally advanced breast cancer in a phase II randomized trial. Clin Cancer Res 2008; 14: 7004-7010.
43. Lucci A, Hall CS, Lodhi AK et al. Circulating tumour cells in non-metastatic breast cancer: a prospective study. Lancet Oncol 2012; 13: 688-695.
44. Franken B, Degroot MR, Mastboom WJ et al. Circulating tumor cells, disease recurrence and survival in newly diagnosed breast cancer. Breast Cancer Res 2012; 14: R133.
45. Rack B, Schindlbeck C, Juckstock J et al. Circulating tumor cells predict survival in early average-to-high risk breast cancer patients. J Natl Cancer Inst 2014; 106: pii: dju066.
46. Ignatiadis M, Riethdorf S, Bidard FC et al. International study on inter-reader variability for circulating tumor cells in breast cancer. Breast Cancer Res 2014; 16: R43.
47. Meng S, Tripathy D, Shete S et al. HER-2 gene amplification can be acquired as breast cancer progresses. Proc Natl Acad Sci USA 2004; 101: 9393-9398.
48. Fehm T, Muller V, Aktas B et al. HER2 status of circulating tumor cells in patients with metastatic breast cancer: a prospective, multicenter trial. Breast Cancer Res Treat 2010; 124: 403-412.
49. Riethdorf S, Muller V, Zhang L et al. Detection and HER2 expression of circulating tumor cells: prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res 2010; 16: 2634-2645.
50. Ignatiadis M, Kallergi G, Ntoulia M et al. Prognostic value of the molecular detection of circulating tumor cells using a multimarker reverse transcription-PCR assay for cytokeratin 19, mammaglobin A, and HER2 in early breast cancer. Clin Cancer Res 2008; 14: 2593-2600.
51. Ignatiadis M, Rothe F, Chaboteaux C et al. HER2-positive circulating tumor cells in breast cancer. PLoS One 2011; 6: e15624.
52. Pestrin M, Bessi S, Puglisi F 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: 283-289.
53. Swennenhuis JF, Tibbe AG, Levink R et al. Characterization of circulating tumor cells by fluorescence in situ hybridization. Cytometry A 2009; 75: 520-527.
54. Paoletti C, Brown M, Muniz M et al. Multi-parameter molecular characterization of circulating tumor cells (CTC): development of a CTC-endocrine therapy index (CTC-ETI). Cancer Res 2011; (Suppl 8).
55. Maheswaran S, Sequist LV, Nagrath S et al. Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 2008; 359: 366-377.
56. Jiang Y, Palma JF, Agus DB et al. Detection of androgen receptor mutations in circulating tumor cells in castration-resistant prostate cancer. Clin Chem 2010; 56: 1492-1495.
57. Miyamoto DT, Lee RJ, Stott SL et al. Androgen receptor signaling in circulating tumor cells as a marker of hormonally responsive prostate cancer. Cancer Discov 2012; 2: 995-1003.
58. Markou A, Strati A, Malamos N et al. Molecular characterization of circulating tumor cells in breast cancer by a liquid bead array hybridization assay. Clin Chem 2011; 57: 421-430.
59. Powell AA, Talasaz AH, Zhang H et al. Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines. PLoS One 2012; 7: e33788.
60. Heitzer E, Auer M, Gasch C et al. Complex tumor genomes inferred from single circulating tumor cells by array-CGH and next-generation sequencing. Cancer Res 2013; 73: 2965-2975.
61. Peeters DJ, De Laere B, Van den Eynden GG et al. Semiautomated isolation and molecular characterisation of single or highly purified tumour cells from CellSearch enriched blood samples using dielectrophoretic cell sorting. Br J Cancer 2013; 108: 1358-1367.
62. Talasaz AH, Powell AA, Huber DE et al. Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proc Natl Acad Sci USA 2009; 106: 3970-3975.
63. Lohr JG, Adalsteinsson VA, Cibulskis K et al. Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer. Nat Biotechnol 2014; 32: 479-484.
64. Hou Y, Song L, Zhu P et al. Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm. Cell 2012; 148: 873-885.
65. Zong C, Lu S, Chapman AR, Xie XS. Genome-wide detection of single-nucleotide and copy-number variations of a single human cell. Science 2012; 338: 1622-1626.
66. Wang Y, Waters J, Leung ML et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 2014; 512: 155-160.
67. Yu M, Bardia A, Aceto N et al. Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 2014; 345: 216-220.
68. Robinson DR, Wu YM, Vats P et al. Activating ESR1 mutations in hormoneresistant metastatic breast cancer. Nat Genet 2013; 45: 1446-1451.
69. Toy W, Shen Y, Won H et al. ESR1 ligand-binding domain mutations in hormoneresistant breast cancer. Nat Genet 2013; 45: 1439-1445.
70. Baccelli I, Schneeweiss A, Riethdorf S 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: 539-544.
71. Hodgkinson CL, Morrow CJ, Li Y et al. Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer. Nat Med 2014; 20: 897-903.
72. Gormally E, Caboux E, Vineis P, Hainaut P. Circulating free DNA in plasma or serum as biomarker of carcinogenesis: practical aspects and biological significance. Mutat Res 2007; 635: 105-117.
73. Anker P, Mulcahy H, Chen XQ, Stroun M. Detection of circulating tumour DNA in the blood (plasma/serum) of cancer patients. Cancer Metastasis Rev 1999; 18: 65-73.
74. Jahr S, Hentze H, Englisch S et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res 2001; 61: 1659-1665.
75. Mouliere F, Robert B, Arnau PE et al. High fragmentation characterizes tumourderived circulating DNA. PLoS One 2011; 6: e23418.
76. Stroun M, Lyautey J, Lederrey C et al. About the possible origin and mechanism of circulating DNA apoptosis and active DNA release. Clin Chim Acta 2001; 313: 139-142.
77. Bettegowda C, Sausen M, Leary RJ et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 2014; 6: 224ra24.
78. Dawson SJ, Tsui DW, Murtaza M et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med 2013; 368: 1199-1209.
79. Punnoose EA, Atwal S, Liu W et al. 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 2012; 18: 2391-2401.
80. El Messaoudi S, Rolet F, Mouliere F, Thierry AR. Circulating cell free DNA: preanalytical considerations. Clin Chim Acta 2013; 424: 222-230.
81. McBride DJ, Orpana AK, Sotiriou C et al. Use of cancer-specific genomic rearrangements to quantify disease burden in plasma from patients with solid tumors. Genes Chromosomes Cancer 2010; 49: 1062-1069.
82. Leary RJ, Kinde I, Diehl F et al. Development of personalized tumor biomarkers using massively parallel sequencing. Sci Transl Med 2010; 2: 20ra14.
83. Board RE, Wardley AM, Dixon JM et al. Detection of PIK3CA mutations in circulating free DNA in patients with breast cancer. Breast Cancer Res Treat 2010; 120: 461-467.
84. Chen Z, Feng J, Buzin CH et al. Analysis of cancer mutation signatures in blood by a novel ultra-sensitive assay: monitoring of therapy or recurrence in nonmetastatic breast cancer. PLoS One 2009; 4: e7220.
85. Diehl F, Schmidt K, Choti MA et al. Circulating mutant DNA to assess tumor dynamics. Nat Med 2008; 14: 985-990.
86. Higgins MJ, Jelovac D, Barnathan E et al. Detection of tumor PIK3CA status in metastatic breast cancer using peripheral blood. Clin Cancer Res 2012; 18: 3462-3469.
87. Forshew T, Murtaza M, Parkinson C et al. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci Transl Med 2012; 4: 136ra68.
88. Yung TK, Chan KC, Mok TS et al. Single-molecule detection of epidermal growth factor receptor mutations in plasma by microfluidics digital PCR in non-small cell lung cancer patients. Clin Cancer Res 2009; 15: 2076-2084.
89. Beaver JA, Jelovac D, Balukrishna S et al. Detection of cancer DNA in plasma of early stage breast cancer patients. Clin Cancer Res 2014; 20: 2643-2650.
90. Newman AM, Bratman SV, To J et al. An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nat Med 2014; 20: 548-554.
91. Rothe F, Laes J, Lambrechts D et al. Plasma circulating tumor DNA as an alternative to metastatic biopsies for mutational analysis in breast cancer. Ann Oncol 2014; 25: 1959-1965.
92. Carreira S, Romanel A, Goodall J et al. Tumor clone dynamics in lethal prostate cancer. Sci Transl Med 2014; 6: 254ra125.
93. Murtaza M, Dawson SJ, Tsui DW et al. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 2013; 497: 108-112.
94. Chan KC, Jiang P, Zheng YW et al. Cancer genome scanning in plasma: detection of tumor-associated copy number aberrations, single-nucleotide variants, and tumoral heterogeneity by massively parallel sequencing. Clin Chem 2013; 59: 211-224.
95. Leary RJ, Sausen M, Kinde I et al. Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing. Sci Transl Med 2012; 4: 162ra154.
96. Heitzer E, Ulz P, Belic J et al. Tumor-associated copy number changes in the circulation of patients with prostate cancer identified through whole-genome sequencing. Genome Med 2013; 5: 30.
97. Chan KC, Jiang P, Chan CW et al. Noninvasive detection of cancer-associated genome-wide hypomethylation and copy number aberrations by plasma DNA bisulfite sequencing. Proc Natl Acad Sci USA 2013; 110: 18761-18768.
98. Schwarzenbach H, Eichelser C, Kropidlowski J et al. Loss of heterozygosity at tumor suppressor genes detectable on fractionated circulating cell-free tumor DNA as indicator of breast cancer progression. Clin Cancer Res 2012; 18: 5719-5730.
99. Shi J, Liu Q, Sommer SS. Detection of ultrarare somatic mutation in the human TP53 gene by bidirectional pyrophosphorolysis-activated polymerization allelespecific amplification. Hum Mutat 2007; 28: 131-136.
100. Vogelstein B, Kinzler KW. Digital PCR. Proc Natl Acad Sci USA 1999; 96: 9236-9241.
101. Hindson BJ, Ness KD, Masquelier DA et al. High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal Chem 2011; 83: 8604-8610.
102. Wang J, Ramakrishnan R, Tang Z et al. Quantifying EGFR alterations in the lung cancer genome with nanofluidic digital PCR arrays. Clin Chem 2010; 56: 623-632.
103. Dressman D, Yan H, Traverso G et al. Transforming single DNA molecules into fluorescent magnetic particles for detection and enumeration of genetic variations. Proc Natl Acad Sci USA 2003; 100: 8817-8822.
104. Kinde I, Wu J, Papadopoulos N et al. Detection and quantification of rare mutations with massively parallel sequencing. Proc Natl Acad Sci USA 2011; 108: 9530-9535.
105. Shaw JA, Page K, Blighe K et al. Genomic analysis of circulating cell-free DNA infers breast cancer dormancy. Genome Res 2012; 22: 220-231.
106. Thierry AR, Mouliere F, El Messaoudi S et al. Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA. Nat Med 2014; 20: 430-435.
107. Mattos-Arruda L, Weigelt B, Cortes J et al. Capturing intra-tumor genetic heterogeneity by de novo mutation profiling of circulating cell-free tumor DNA: a proof-of-principle. Ann Oncol 2014; 25: 1729-1735.
108. Rago C, Huso DL, Diehl F et al. Serial assessment of human tumor burdens in mice by the analysis of circulating DNA. Cancer Res 2007; 67: 9364-9370.
109. Nygaard AD, Garm Spindler KL, Pallisgaard N et al. The prognostic value of KRAS mutated plasma DNA in advanced non-small cell lung cancer. Lung Cancer 2013; 79: 312-317.
110. Diaz LA, Jr, Williams RT, Wu J et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012; 486: 537-540.
111. Misale S, Yaeger R, Hobor S et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012; 486: 532-6.
112. Misale S, Arena S, Lamba S et al. Blockade of EGFR and MEK intercepts heterogeneous mechanisms of acquired resistance to anti-EGFR therapies in colorectal cancer. Sci Transl Med 2014; 6: 224ra26.
113. Oxnard GR, Paweletz CP, Kuang Y et al. Noninvasive detection of response and resistance in EGFR-mutant lung cancer using quantitative next-generation genotyping of cell-free plasma DNA. Clin Cancer Res 2014; 20: 1698-1705.
114. Bardelli A, Corso S, Bertotti A et al. Amplification of the MET receptor drives resistance to anti-EGFR therapies in colorectal cancer. Cancer Discov 2013; 3: 658-673.
115. Hughes T, Deininger M, Hochhaus A et al. Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood 2006; 108: 28-37.
116. Grimwade D, Vyas P, Freeman S. Assessment of minimal residual disease in acute myeloid leukemia. Curr Opin Oncol 2010; 22: 656-663.