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Potential clinical applications of circulating cell-free DNA in ovarian cancer patients

Published online by Cambridge University Press:  18 December 2018

Ana Barbosa
Affiliation:
Cancer Genetics Group, IPO-Porto Research Center (CI-IPOP), Portuguese Oncology Institute of Porto (IPO-Porto), Porto, Portugal
Ana Peixoto
Affiliation:
Department of Genetics, Portuguese Oncology Institute of Porto (IPO-Porto), Porto, Portugal
Pedro Pinto
Affiliation:
Cancer Genetics Group, IPO-Porto Research Center (CI-IPOP), Portuguese Oncology Institute of Porto (IPO-Porto), Porto, Portugal
Manuela Pinheiro
Affiliation:
Cancer Genetics Group, IPO-Porto Research Center (CI-IPOP), Portuguese Oncology Institute of Porto (IPO-Porto), Porto, Portugal
Manuel R. Teixeira*
Affiliation:
Cancer Genetics Group, IPO-Porto Research Center (CI-IPOP), Portuguese Oncology Institute of Porto (IPO-Porto), Porto, Portugal Department of Genetics, Portuguese Oncology Institute of Porto (IPO-Porto), Porto, Portugal Department of Pathology and Molecular Immunology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal
*
Author for correspondence: Manuel R. Teixeira, E-mail: manuel.teixeira@ipoporto.min-saude.pt

Abstract

Circulating cell-free DNA (cfDNA) consists of small fragments of DNA that circulate freely in the bloodstream. In cancer patients, a fraction of cfDNA is derived from tumour cells, therefore containing the same genetic and epigenetic alterations, and is termed circulating cell-free tumour DNA. The potential use of cfDNA, the so-called ‘liquid biopsy’, as a non-invasive cancer biomarker has recently received a lot of attention. The present review will focus on studies concerning the potential clinical applications of cfDNA in ovarian cancer patients.

Type
Unsolicited Review
Copyright
Copyright © Cambridge University Press 2018 

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References

1.Mandel, P and Metais, P (1948) Les acides nucléiques du plasma sanguin chez l'homme. Comptes Rendus Des Seances De La Societe De Biologie Et De Ses Filiales 142, 241243.Google Scholar
2.Tan, EM et al. (1966) Deoxybonucleic acid (DNA) and antibodies to DNA in the serum of patients with systemic lupus erythematosus. Journal of Clinical Investigation 45, 17321740.Google Scholar
3.Leon, SA et al. (1977) Free DNA in the serum of cancer patients and the effect of therapy. Cancer Research 37, 646650.Google Scholar
4.Shapiro, B et al. (1983) Determination of circulating DNA levels in patients with benign or malignant gastrointestinal disease. Cancer 51, 21162120.Google Scholar
5.Stroun, M et al. (1987) Isolation and characterization of DNA from the plasma of cancer patients. European Journal of Cancer & Clinical Oncology 23, 707712.Google Scholar
6.Stroun, M et al. (1989) Neoplastic characteristics of the DNA found in the plasma of cancer patients. Oncology 46, 318322.Google Scholar
7.Sorenson, GD et al. (1994) Soluble normal and mutated DNA sequences from single-copy genes in human blood. Cancer Epidemiology, Biomarkers & Prevention 3, 6771.Google Scholar
8.Chen, XQ et al. (1996) Microsatellite alterations in plasma DNA of small cell lung cancer patients. Nature Medicine 2, 10331035.Google Scholar
9.Nawroz, H et al. (1996) Microsatellite alterations in serum DNA of head and neck cancer patients. Nature Medicine 2, 10351037.Google Scholar
10.Silva, JM et al. (1999) TP53 gene mutations in plasma DNA of cancer patients. Genes Chromosomes and Cancer 24, 160161.Google Scholar
11.Esteller, M et al. (1999) Detection of aberrant promoter hypermethylation of tumor suppressor genes in serum DNA from non-small cell lung cancer patients. Cancer Research 59, 6770.Google Scholar
12.Wong, IH et al. (1999) Detection of aberrant p16 methylation in the plasma and serum of liver cancer patients. Cancer Research 59, 7173.Google Scholar
13.Marzese, DM et al. (2013) Diagnostic and prognostic value of circulating tumor-related DNA in cancer patients. Expert Review of Molecular Diagnostics 13, 827844.Google Scholar
14.Burrell, RA et al. (2013) The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338345.Google Scholar
15.Diehl, F et al. (2008) Circulating mutant DNA to assess tumor dynamics. Nature Medicine 14, 985990.Google Scholar
16.Gautschi, O et al. (2004) Circulating deoxyribonucleic Acid as prognostic marker in non-small-cell lung cancer patients undergoing chemotherapy. Journal of Clinical Oncology 22, 41574164.Google Scholar
17.Jahr, S et al. (2001) DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Research 61, 16591665.Google Scholar
18.Alix-Panabieres, C and Pantel, K (2016) Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discovery 6, 479491.Google Scholar
19.Suzuki, N et al. (2008) Characterization of circulating DNA in healthy human plasma. Clinica Chimica Acta 387, 5558.Google Scholar
20.Stroun, M et al. (2001) About the possible origin and mechanism of circulating DNA apoptosis and active DNA release. Clinica Chimica Acta 313, 139142.Google Scholar
21.Plaks, V et al. (2013) Cancer. Circulating tumor cells. Science 341, 11861188.Google Scholar
22.Alix-Panabieres, C and Pantel, K (2013) Circulating tumor cells: liquid biopsy of cancer. Clinical Chemistry 59, 110118.Google Scholar
23.Sorenson, GD (2000) Detection of mutated KRAS2 sequences as tumor markers in plasma/serum of patients with gastrointestinal cancer. Clinical Cancer Research 6, 21292137.Google Scholar
24.Anker, P et al. (1975) Spontaneous release of DNA by human blood lymphocytes as shown in an in vitro system. Cancer Research 35, 23752382.Google Scholar
25.Lo, YM et al. (1999) Rapid clearance of fetal DNA from maternal plasma. American Journal of Human Genetics 64, 218224.Google Scholar
26.Fleischhacker, M and Schmidt, B (2007) Circulating nucleic acids (CNAs) and cancer--a survey. Biochimica et Biophysica Acta 1775, 181232.Google Scholar
27.Tsumita, T and Iwanaga, M (1963) Fate of injected deoxyribonucleic acid in mice. Nature 198, 10881089.Google Scholar
28.Chused, TM et al. (1972) The clearance and localization of nucleic acids by New Zealand and normal mice. Clinical and Experimental Immunology 12, 465476.Google Scholar
29.Emlen, W and Mannik, M (1978) Kinetics and mechanisms for removal of circulating single-stranded DNA in mice. Journal of Experimental Medicine 147, 684699.Google Scholar
30.Garcia-Olmo, D and Garcia-Olmo, DC (2001) Functionality of circulating DNA: the hypothesis of genometastasis. Annals of the New York Academy of Sciences 945, 265275.Google Scholar
31.Ferlay, J et al. (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. International Journal of Cancer 136, E359E386.Google Scholar
32.Guppy, AE et al. (2005) Epithelial ovarian cancer: a review of current management. Clinical Oncology (Royal College of Radiologists) 17, 399411.Google Scholar
33.Prat, J (2012) Ovarian carcinomas: five distinct diseases with different origins, genetic alterations, and clinicopathological features. Virchows Archiv 460, 237249.Google Scholar
34.Seidman, J (2014) Advances in sub-classification of ovarian carcinomas by cell type: an update. Diagnostic Histopathology/Published in Association With the Pathological Society of Great Britain and Ireland 20, 351356.Google Scholar
35.Kanchi, KL et al. (2014) Integrated analysis of germline and somatic variants in ovarian cancer. Nature Communications 5, 3156.Google Scholar
36.Meinhold-Heerlein, I and Hauptmann, S (2014) The heterogeneity of ovarian cancer. Archives of Gynecology and Obstetrics 289, 237239.Google Scholar
37.Cancer Genome Atlas Research, N. (2011) Integrated genomic analyses of ovarian carcinoma. Nature 474, 609615.Google Scholar
38.Bast, RC Jr, et al. (2009) The biology of ovarian cancer: new opportunities for translation. Nature Reviews Cancer 9, 415428.Google Scholar
39.Barton, CA et al. (2008) DNA methylation changes in ovarian cancer: implications for early diagnosis, prognosis and treatment. Gynecologic Oncology 109, 129139.Google Scholar
40.Bai, H et al. (2016) Genetic and epigenetic heterogeneity of epithelial ovarian cancer and the clinical implications for molecular targeted therapy. Journal of Cellular and Molecular Medicine 20, 581593.Google Scholar
41.Sozzi, G et al. (2001) Analysis of circulating tumor DNA in plasma at diagnosis and during follow-up of lung cancer patients. Cancer Research 61, 46754678.Google Scholar
42.Mori, T et al. (2005) Predictive utility of circulating methylated DNA in serum of melanoma patients receiving biochemotherapy. Journal of Clinical Oncology 23, 93519358.Google Scholar
43.Gautschi, O et al. (2007) Origin and prognostic value of circulating KRAS mutations in lung cancer patients. Cancer Letters 254, 265273.Google Scholar
44.Kuang, Y et al. (2009) Noninvasive detection of EGFR T790M in gefitinib or erlotinib resistant non-small cell lung cancer. Clinical Cancer Research 15, 26302636.Google Scholar
45.Misale, S et al. (2012) Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 486, 532536.Google Scholar
46.Dawson, SJ et al. (2013) Analysis of circulating tumor DNA to monitor metastatic breast cancer. New England Journal of Medicine 368, 11991209.Google Scholar
47.Hamakawa, T et al. (2015) Monitoring gastric cancer progression with circulating tumour DNA. British Journal of Cancer 112, 352356.Google Scholar
48.Garcia-Murillas, I et al. (2015) Mutation tracking in circulating tumor DNA predicts relapse in early breast cancer. Science Translational Medicine 7, 302ra133.Google Scholar
49.Chen, X et al. (1999) Detecting tumor-related alterations in plasma or serum DNA of patients diagnosed with breast cancer. Clinical Cancer Research 5, 22972303.Google Scholar
50.Reinert, T et al. (2016) Analysis of circulating tumour DNA to monitor disease burden following colorectal cancer surgery. Gut 65, 625634.Google Scholar
51.Visintin, I et al. (2008) Diagnostic markers for early detection of ovarian cancer. Clinical Cancer Research 14, 10651072.Google Scholar
52.Ricci, S and Shih, I-M (2013) Screening for ovarian cancer: a reality check. Current Obstetrics and Gynecology Reports 2, 7375.Google Scholar
53.Duffy, MJ et al. (2005) CA125 in ovarian cancer: European Group on Tumor Markers guidelines for clinical use. International Journal of Gynecological Cancer 15, 679691.Google Scholar
54.DePriest, PD and DeSimone, CP (2003) Ultrasound screening for the early detection of ovarian cancer. Journal of Clinical Oncology 21(Suppl. 10), 194s199s.Google Scholar
55.Schwartz, PE (2002) Current diagnosis and treatment modalities for ovarian cancer. Cancer Treatment and Research 107, 99118.Google Scholar
56.Reade, CJ et al. (2013) Risks and benefits of screening asymptomatic women for ovarian cancer: a systematic review and meta-analysis. Gynecologic Oncology 130, 674681.Google Scholar
57.Kamat, AA et al. (2006) Quantification of total plasma cell-free DNA in ovarian cancer using real-time PCR. Annals of the New York Academy of Sciences 1075, 230234.Google Scholar
58.Kamat, AA et al. (2010) Plasma cell-free DNA in ovarian cancer: an independent prognostic biomarker. Cancer 116, 19181925.Google Scholar
59.Shao, X et al. (2015) Quantitative analysis of cell-free DNA in ovarian cancer. Oncology Letters 10, 34783482.Google Scholar
60.Zachariah, RR et al. (2008) Levels of circulating cell-free nuclear and mitochondrial DNA in benign and malignant ovarian tumors. Obstetrics & Gynecology 112, 843850.Google Scholar
61.Zhou, Q et al. (2016) Circulating cell free DNA as the diagnostic marker for ovarian cancer: a systematic review and meta-analysis. PLoS ONE 11, e0155495.Google Scholar
62.Otsuka, J et al. (2004) Detection of p53 mutations in the plasma DNA of patients with ovarian cancer. International Journal of Gynecological Cancer 14, 459464.Google Scholar
63.Swisher, EM et al. (2005) Tumor-specific p53 sequences in blood and peritoneal fluid of women with epithelial ovarian cancer. American Journal of Obstetrics and Gynecology 193(3 Pt 1), 662667.Google Scholar
64.Pereira, E et al. (2015) Personalized circulating tumor DNA biomarkers dynamically predict treatment response and survival in gynecologic cancers. PLoS ONE 10, e0145754.Google Scholar
65.Phallen, J et al. (2017) Direct detection of early-stage cancers using circulating tumor DNA. Science Translational Medicine 9, eaan2415.Google Scholar
66.Harris, FR et al. (2016) Quantification of somatic chromosomal rearrangements in circulating cell-free DNA from ovarian cancers. Scientific Reports 6, 29831.Google Scholar
67.Cohen, PA et al. (2016) Abnormal plasma DNA profiles in early ovarian cancer using a non-invasive prenatal testing platform: implications for cancer screening. BMC Medicine 14, 126.Google Scholar
68.No, JH et al. (2012) Cell-free DNA level as a prognostic biomarker for epithelial ovarian cancer. Anticancer Research 32, 34673471.Google Scholar
69.Vanderstichele, A et al. (2017) Chromosomal instability in cell-free DNA as a highly specific biomarker for detection of ovarian cancer in women with adnexal masses. Clinical Cancer Research 23, 22232231.Google Scholar
70.Wu, Y et al. (2014) Aberrant methylation of RASSF2A in tumors and plasma of patients with epithelial ovarian cancer. Asian Pacific Journal of Cancer Prevention 15, 11711176.Google Scholar
71.Ibanez de Caceres, I et al. (2004) Tumor cell-specific BRCA1 and RASSF1A hypermethylation in serum, plasma, and peritoneal fluid from ovarian cancer patients. Cancer Research 64, 64766481.Google Scholar
72.Melnikov, A et al. (2009) Differential methylation profile of ovarian cancer in tissues and plasma. The Journal of Molecular Diagnostics 11, 6065.Google Scholar
73.Liggett, TE et al. (2011) Distinctive DNA methylation patterns of cell-free plasma DNA in women with malignant ovarian tumors. Gynecologic Oncology 120, 113120.Google Scholar
74.Aravanis, AM et al. (2017) Next-Generation sequencing of circulating tumor DNA for early cancer detection. Cell 168, 571574.Google Scholar
75.Cohen, JD et al. (2018) Detection and localization of surgically resectable cancers with a multi-analyte blood test. Science 359, 926930.Google Scholar
76.Holschneider, CH and Berek, JS (2000) Ovarian cancer: epidemiology, biology, and prognostic factors. Seminars in Surgical Oncology 19, 310.Google Scholar
77.Agarwal, R and Kaye, SB (2005) Prognostic factors in ovarian cancer: how close are we to a complete picture? Annals of Oncology 16, 46.Google Scholar
78.Capizzi, E et al. (2008) Quantification of free plasma DNA before and after chemotherapy in patients with advanced epithelial ovarian cancer. Diagnostic Molecular Pathology 17, 3438.Google Scholar
79.Wimberger, P et al. (2011) Impact of platinum-based chemotherapy on circulating nucleic acid levels, protease activities in blood and disseminated tumor cells in bone marrow of ovarian cancer patients. International Journal of Cancer 128, 25722580.Google Scholar
80.Steffensen, KD et al. (2014) Prognostic importance of cell-free DNA in chemotherapy resistant ovarian cancer treated with bevacizumab. European Journal of Cancer 50, 26112618.Google Scholar
81.Dobrzycka, B et al. (2011) Circulating free DNA and p53 antibodies in plasma of patients with ovarian epithelial cancers. Annals of Oncology 22, 11331140.Google Scholar
82.Parkinson, CA et al. (2016) Exploratory analysis of TP53 mutations in circulating tumour DNA as biomarkers of treatment response for patients with relapsed high-grade serous ovarian carcinoma: a retrospective study. PLoS Medicine 13, e1002198.Google Scholar
83.Gifford, G et al. (2004) The acquisition of hMLH1 methylation in plasma DNA after chemotherapy predicts poor survival for ovarian cancer patients. Clinical Cancer Research 10, 44204426.Google Scholar
84.Aletti, GD et al. (2007) Current management strategies for ovarian cancer. Mayo Clinic Proceedings 82, 751770.Google Scholar
85.Jelovac, D and Armstrong, DK (2011) Recent progress in the diagnosis and treatment of ovarian cancer. CA: A Cancer Journal for Clinicians 61, 183203.Google Scholar
86.Johnson, SW et al. (1993) Mechanisms of drug resistance in ovarian cancer. Cancer 71(Suppl. 2), 644649.Google Scholar
87.Liu, X et al. (2015) Oncogenes associated with drug resistance in ovarian cancer. Journal of Cancer Research and Clinical Oncology 141, 381395.Google Scholar
88.Kamat, AA et al. (2006) Circulating cell-free DNA: a novel biomarker for response to therapy in ovarian carcinoma. Cancer Biology & Therapy 5, 13691374.Google Scholar
89.Choudhuri, S et al. (2014) A repertoire of biomarkers helps in detection and assessment of therapeutic response in epithelial ovarian cancer. Molecular and Cellular Biochemistry 386, 259269.Google Scholar
90.Murtaza, M et al. (2013) Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 497, 108112.Google Scholar
91.Knudsen, ES and Knudsen, KE (2008) Tailoring to RB: tumour suppressor status and therapeutic response. Nature Reviews Cancer 8, 714724.Google Scholar
92.Martignetti, JA et al. (2014) Personalized ovarian cancer disease surveillance and detection of candidate therapeutic drug target in circulating tumor DNA. Neoplasia (New York, N.Y.) 16, 97103.Google Scholar
93.Christie, EL et al. (2017) Reversion of BRCA1/2 germline mutations detected in circulating tumor DNA from patients with high-grade serous ovarian cancer. Journal of Clinical Oncology 35, 12741280.Google Scholar
94.Weigelt, B et al. (2017) Diverse BRCA1 and BRCA2 reversion mutations in circulating cell-free DNA of therapy-resistant breast or ovarian cancer. Clinical Cancer Research 23, 67086720.Google Scholar
95.Planchard, D et al. (2018) Metastatic non-small cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of Oncology 29(Suppl. 4), iv192iv237.Google Scholar
97.Ledermann, J et al. (2014) Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. The Lancet Oncology 15, 852861.Google Scholar
98.van Schendel, RV et al. (2017) Implementing non-invasive prenatal testing for aneuploidy in a national healthcare system: global challenges and national solutions. BMC Health Services Research 17, 670.Google Scholar
99.Heitzer, E et al. (2017) The potential of liquid biopsies for the early detection of cancer. NPJ Precision Oncology 1, 36.Google Scholar