Cell-free circulating tumour DNA as a liquid biopsy in breast cancer

Molecular Oncology

Volumn 10, Issue 3, 2016, Pages 464-474

  De Mattos Arruda, Leticia ^a,b,c   Caldas, Carlos ^a,d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b VALL D HEBRON UNIVERSITY HOSPITAL   (Spain)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d NIHR Cambridge Biomedical Research Centre   (United Kingdom)

Author keywords

Breast cancer; Circulating cell free tumour DNA; Heterogeneity; Monitoring; Resistance; Stratification

Indexed keywords

CELL FREE CIRCULATING TUMOR DNA; DNA; UNCLASSIFIED DRUG; TUMOR MARKER;

BREAST CANCER; CANCER RECURRENCE; CANCER RESISTANCE; GENOMICS; HUMAN; LIQUID BIOPSY; MINIMAL RESIDUAL DISEASE; PRIORITY JOURNAL; REVIEW; TUMOR BIOPSY; ANIMAL; BIOPSY; BLOOD; BREAST; BREAST NEOPLASMS; FEMALE; GENETICS; HIGH THROUGHPUT SEQUENCING; PATHOLOGY; PROCEDURES;

ANIMALS; BIOMARKERS, TUMOR; BIOPSY; BREAST; BREAST NEOPLASMS; DNA, NEOPLASM; FEMALE; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS;

EID: 84959105405     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2015.12.001     Document Type: Review

References (69)

1. Ali H.R., Rueda O.M., Chin S.F., Curtis C., Dunning M.J., Aparicio S.A., Caldas C. Genome-driven integrated classification of breast cancer validated in over 7,500 samples. Genome Biol. 2014, 15:431.
2. Amant F., Verheecke M., Wlodarska I., Dehaspe L., Brady P., Brison N., Van Den Bogaert K., Dierickx D., Vandecaveye V., Tousseyn T., Moerman P., Vanderstichele A., Vergote I., Neven P., Berteloot P., Putseys K., Danneels L., Vandenberghe P., Legius E., Vermeesch J.R. Presymptomatic identification of cancers in pregnant women during noninvasive prenatal testing. JAMA Oncol. 2015, 1:814-819.
3. Andre F., Bachelot T., Commo F., Campone M., Arnedos M., Dieras V., Lacroix-Triki M., Lacroix L., Cohen P., Gentien D., Adelaide J., Dalenc F., Goncalves A., Levy C., Ferrero J.M., Bonneterre J., Lefeuvre C., Jimenez M., Filleron T., Bonnefoi H. Comparative genomic hybridisation array and DNA sequencing to direct treatment of metastatic breast cancer: a multicentre, prospective trial (SAFIR01/UNICANCER). Lancet Oncol. 2014, 15:267-274.
4. Aparicio S., Caldas C. The implications of clonal genome evolution for cancer medicine. N. Engl. J. Med. 2013, 368:842-851.
5. Arnedos M., Soria J.C., Andre F., Tursz T. Personalized treatments of cancer patients: a reality in daily practice, a costly dream or a shared vision of the future from the oncology community?. Cancer Treat Rev. 2014, 40:1192-1198.
6. Beaver J.A., Jelovac D., Balukrishna S., Cochran R.L., Croessmann S., Zabransky D.J., Wong H.Y., Valda Toro P., Cidado J., Blair B.G., Chu D., Burns T., Higgins M.J., Stearns V., Jacobs L., Habibi M., Lange J., Hurley P.J., Lauring J., VanDenBerg D.A., Kessler J., Jeter S., Samuels M.L., Maar D., Cope L., Cimino-Mathews A., Argani P., Wolff A.C., Park B.H. Detection of cancer DNA in plasma of patients with early-stage breast cancer. Clin. Cancer Res. 2014, 20:2643-2650.
7. Bedard P.L., Hansen A.R., Ratain M.J., Siu L.L. Tumour heterogeneity in the clinic. Nature 2013, 501:355-364.
8. Belic J., Koch M., Ulz P., Auer M., Gerhalter T., Mohan S., Fischereder K., Petru E., Bauernhofer T., Geigl J.B., Speicher M.R., Heitzer E. Rapid identification of plasma DNA samples with increased ctDNA levels by a modified FAST-SeqS approach. Clin. Chem. 2015, 61:838-849.
9. Bettegowda C., Sausen M., Leary R.J., Kinde I., Wang Y., Agrawal N., Bartlett B.R., Wang H., Luber B., Alani R.M., Antonarakis E.S., Azad N.S., Bardelli A., Brem H., Cameron J.L., Lee C.C., Fecher L.A., Gallia G.L., Gibbs P., Le D., Giuntoli R.L., Goggins M., Hogarty M.D., Holdhoff M., Hong S.M., Jiao Y., Juhl H.H., Kim J.J., Siravegna G., Laheru D.A., Lauricella C., Lim M., Lipson E.J., Marie S.K., Netto G.J., Oliner K.S., Olivi A., Olsson L., Riggins G.J., Sartore-Bianchi A., Schmidt K., Shih I.M., Oba-Shinjo S.M., Siena S., Theodorescu D., Tie J., Harkins T.T., Veronese S., Wang T.L., Weingart J.D., Wolfgang C.L., Wood L.D., Xing D., Hruban R.H., Wu J., Allen P.J., Schmidt C.M., Choti M.A., Velculescu V.E., Kinzler K.W., Vogelstein B., Papadopoulos N., Diaz L.A. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci. Transl. Med. 2014, 6:224ra224.
10. Board R.E., Wardley A.M., Dixon J.M., Armstrong A.C., Howell S., Renshaw L., Donald E., Greystoke A., Ranson M., Hughes A., Dive C. Detection of PIK3CA mutations in circulating free DNA in patients with breast cancer. Breast Cancer Res. Treat 2010, 120:461-467.
11. Cancer Genome Atlas, N Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70.
12. Chen W.W., Balaj L., Liau L.M., Samuels M.L., Kotsopoulos S.K., Maguire C.A., Loguidice L., Soto H., Garrett M., Zhu L.D., Sivaraman S., Chen C., Wong E.T., Carter B.S., Hochberg F.H., Breakefield X.O., Skog J. BEAMing and droplet digital PCR analysis of mutant IDH1 mRNA in glioma patient serum and cerebrospinal fluid extracellular vesicles. Mol. Ther. Nucleic Acids 2013, 2:e109.
13. Chen Z., Feng J., Buzin C.H., Liu Q., Weiss L., Kernstine K., Somlo G., Sommer S.S. 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 2009, 4:e7220.
14. Cheng D.T., Mitchell T.N., Zehir A., Shah R.H., Benayed R., Syed A., Chandramohan R., Liu Z.Y., Won H.H., Scott S.N., Brannon A.R., O'Reilly C., Sadowska J., Casanova J., Yannes A., Hechtman J.F., Yao J., Song W., Ross D.S., Oultache A., Dogan S., Borsu L., Hameed M., Nafa K., Arcila M.E., Ladanyi M., Berger M.F. Memorial Sloan Kettering-Integrated Mutation Profiling of Actionable Cancer Targets (MSK-IMPACT): a hybridization capture-based next-generation sequencing clinical assay for solid tumor molecular oncology. J. Mol. Diagn. 2015, 17:251-264.
15. Chu D., Paoletti C., Gersch C., VanDenBerg D., Zabransky D., Cochran R., Wong H.Y., Valda Toro P., Cidado J., Croessmann S., Erlanger B., Cravero K., Kyker-Snowman K., Button B., Parsons H., Dalton W.B., Gillani R., Medford A., Aung K., Tokudome N., Chinnaiyan A., Schott A.F., Robinson D.R., Jacks K., Lauring J., Hurley P.J., Hayes D.F., Rae J.M., Park B.H. ESR1 mutations in circulating plasma tumor DNA from metastatic breast cancer patients. Clin. Cancer Res. 2015 Aug 10, [Epub ahead of print].
16. Cui J., Germer K., Wu T., Wang J., Luo J., Wang S.C., Wang Q., Zhang X. Cross-talk between HER2 and MED1 regulates tamoxifen resistance of human breast cancer cells. Cancer Res. 2012, 72:5625-5634.
17. Curtis C., Shah S.P., Chin S.F., Turashvili G., Rueda O.M., Dunning M.J., Speed D., Lynch A.G., Samarajiwa S., Yuan Y., Graf S., Ha G., Haffari G., Bashashati A., Russell R., McKinney S., Group M., Langerod A., Green A., Provenzano E., Wishart G., Pinder S., Watson P., Markowetz F., Murphy L., Ellis I., Purushotham A., Borresen-Dale A.L., Brenton J.D., Tavare S., Caldas C., Aparicio S. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352.
18. Dawson S.J., Rueda O.M., Aparicio S., Caldas C. A new genome-driven integrated classification of breast cancer and its implications. EMBO J. 2013, 32:617-628.
19. Dawson S.J., Tsui D.W., Murtaza M., Biggs H., Rueda O.M., Chin S.F., Dunning M.J., Gale D., Forshew T., Mahler-Araujo B., Rajan S., Humphray S., Becq J., Halsall D., Wallis M., Bentley D., Caldas C., Rosenfeld N. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl. J. Med. 2013, 368:1199-1209.
20. De Mattos-Arruda L., Cortes J., Santarpia L., Vivancos A., Tabernero J., Reis-Filho J.S., Seoane J. Circulating tumour cells and cell-free DNA as tools for managing breast cancer. Nat. Rev. Clin. Oncol. 2013, 10:377-389.
21. De Mattos-Arruda L., Mayor R., Ng C.K., Weigelt B., Martinez-Ricarte F., Torrejon D., Oliveira M., Arias A., Raventos C., Tang J., Guerini-Rocco E., Martinez-Saez E., Lois S., Marin O., de la Cruz X., Piscuoglio S., Towers R., Vivancos A., Peg V., Cajal S.R., Carles J., Rodon J., Gonzalez-Cao M., Tabernero J., Felip E., Sahuquillo J., Berger M.F., Cortes J., Reis-Filho J.S., Seoane J. Cerebrospinal fluid-derived circulating tumour DNA better represents the genomic alterations of brain tumours than plasma. Nat. Commun. 2015, 6:8839.
22. De Mattos-Arruda L., Rodon J. Pilot studies for personalized cancer medicine: focusing on the patient for treatment selection. Oncologist 2013, 18:1180-1188.
23. De Mattos-Arruda L., Weigelt B., Cortes J., Won H.H., Ng C.K., Nuciforo P., Bidard F.C., Aura C., Saura C., Peg V., Piscuoglio S., Oliveira M., Smolders Y., Patel P., Norton L., Tabernero J., Berger M.F., Seoane J., Reis-Filho J.S. 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.
24. Diaz L.A., Bardelli A. Liquid biopsies: genotyping circulating tumor DNA. J. Clin. Oncol. 2014, 32:579-586.
25. Dienstmann R., Serpico D., Rodon J., Saura C., Macarulla T., Elez E., Alsina M., Capdevila J., Perez-Garcia J., Sanchez-Olle G., Aura C., Prudkin L., Landolfi S., Hernandez-Losa J., Vivancos A., Tabernero J. Molecular profiling of patients with colorectal cancer and matched targeted therapy in phase I clinical trials. Mol. Cancer Ther. 2012, 11:2062-2071.
26. Dvinge H., Git A., Graf S., Salmon-Divon M., Curtis C., Sottoriva A., Zhao Y., Hirst M., Armisen J., Miska E.A., Chin S.F., Provenzano E., Turashvili G., Green A., Ellis I., Aparicio S., Caldas C. The shaping and functional consequences of the microRNA landscape in breast cancer. Nature 2013, 497:378-382.
27. Forshew T., Murtaza M., Parkinson C., Gale D., Tsui D.W., Kaper F., Dawson S.J., Piskorz A.M., Jimenez-Linan M., Bentley D., Hadfield J., May A.P., Caldas C., Brenton J.D., Rosenfeld N. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci. Transl. Med. 2012, 4:136ra168.
28. Frenel J.S., Carreira S., Goodall J., Roda Perez D., Perez Lopez R., Tunariu N., Riisnaes R., Miranda S., Figueiredo I., Nava Rodrigues D., Smith A., Leux C., Garcia-Murillas I., Ferraldeschi R., Lorente D., Mateo J., Ong M., Yap T.A., Banerji U., Gasi Tandefelt D., Turner N., Attard G., de Bono J.S. Serial next generation sequencing of circulating cell free DNA evaluating tumour clone response to molecularly targeted drug administration. Clin. Cancer Res. 2015, 21:4586-4596.
29. Garcia-Murillas I., Schiavon G., Weigelt B., Ng C., Hrebien S., Cutts R.J., Cheang M., Osin P., Nerurkar A., Kozarewa I., Garrido J.A., Dowsett M., Reis-Filho J.S., Smith I.E., Turner N.C. Mutation tracking in circulating tumor DNA predicts relapse in early breast cancer. Sci. Transl. Med. 2015, 7:302ra133.
30. Gerlinger M., Rowan A.J., Horswell S., Larkin J., Endesfelder D., Gronroos E., Martinez P., Matthews N., Stewart A., Tarpey P., Varela I., Phillimore B., Begum S., McDonald N.Q., Butler A., Jones D., Raine K., Latimer C., Santos C.R., Nohadani M., Eklund A.C., Spencer-Dene B., Clark G., Pickering L., Stamp G., Gore M., Szallasi Z., Downward J., Futreal P.A., Swanton C. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 2012, 366:883-892.
31. Gevensleben H., Garcia-Murillas I., Graeser M.K., Schiavon G., Osin P., Parton M., Smith I.E., Ashworth A., Turner N.C. Noninvasive detection of HER2 amplification with plasma DNA digital PCR. Clin. Cancer Res. 2013, 19:3276-3284.
32. Guttery D.S., Page K., Hills A., Woodley L., Marchese S.D., Rghebi B., Hastings R.K., Luo J., Pringle J.H., Stebbing J., Coombes R.C., Ali S., Shaw J.A. Noninvasive detection of activating Estrogen Receptor 1 (ESR1) mutations in estrogen receptor-positive metastatic breast cancer. Clin. Chem. 2015, 61:974-982.
33. Haber D.A., Velculescu V.E. Blood-based analyses of cancer: circulating tumor cells and circulating tumor DNA. Cancer Discov. 2014, 4:650-661.
34. Heidary M., Auer M., Ulz P., Heitzer E., Petru E., Gasch C., Riethdorf S., Mauermann O., Lafer I., Pristauz G., Lax S., Pantel K., Geigl J.B., Speicher M.R. The dynamic range of circulating tumor DNA in metastatic breast cancer. Breast Cancer Res. 2014, 16:421.
35. Heitzer E., Auer M., Hoffmann E.M., Pichler M., Gasch C., Ulz P., Lax S., Waldispuehl-Geigl J., Mauermann O., Mohan S., Pristauz G., Lackner C., Hofler G., Eisner F., Petru E., Sill H., Samonigg H., Pantel K., Riethdorf S., Bauernhofer T., Geigl J.B., Speicher M.R. Establishment of tumor-specific copy number alterations from plasma DNA of patients with cancer. Int. J. Cancer 2013, 133:346-356.
36. Higgins M.J., Jelovac D., Barnathan E., Blair B., Slater S., Powers P., Zorzi J., Jeter S.C., Oliver G.R., Fetting J., Emens L., Riley C., Stearns V., Diehl F., Angenendt P., Huang P., Cope L., Argani P., Murphy K.M., Bachman K.E., Greshock J., Wolff A.C., Park B.H. Detection of tumor PIK3CA status in metastatic breast cancer using peripheral blood. Clin. Cancer Res. 2012, 18:3462-3469.
37. Jahr S., Hentze H., Englisch S., Hardt D., Fackelmayer F.O., Hesch R.D., Knippers R. 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.
38. Janku F., Angenendt P., Tsimberidou A.M., Fu S., Naing A., Falchook G.S., Hong D.S., Holley V.R., Cabrilo G., Wheler J.J., Piha-Paul S.A., Zinner R.G., Bedikian A.Y., Overman M.J., Kee B.K., Kim K.B., Kopetz E.S., Luthra R., Diehl F., Meric-Bernstam F., Kurzrock R. Actionable mutations in plasma cell-free DNA in patients with advanced cancers referred for experimental targeted therapies. Oncotarget 2015, 6:12809-12821.
39. Lavon I., Refael M., Zelikovitch B., Shalom E., Siegal T. Serum DNA can define tumor-specific genetic and epigenetic markers in gliomas of various grades. Neuro Oncol. 2010, 12:173-180.
40. Le Tourneau C., Delord J.P., Goncalves A., Gavoille C., Dubot C., Isambert N., Campone M., Tredan O., Massiani M.A., Mauborgne C., Armanet S., Servant N., Bieche I., Bernard V., Gentien D., Jezequel P., Attignon V., Boyault S., Vincent-Salomon A., Servois V., Sablin M.P., Kamal M., Paoletti X. Molecularly targeted therapy based on tumour molecular profiling versus conventional therapy for advanced cancer (SHIVA): a multicentre, open-label, proof-of-concept, randomised, controlled phase 2 trial. Lancet Oncol. 2015, 16:1324-1334. investigators, S.
41. Leary R.J., Kinde I., Diehl F., Schmidt K., Clouser C., Duncan C., Antipova A., Lee C., McKernan K., De La Vega F.M., Kinzler K.W., Vogelstein B., Diaz L.A., Velculescu V.E. Development of personalized tumor biomarkers using massively parallel sequencing. Sci. Transl. Med. 2010, 2:20ra14.
42. Leary R.J., Sausen M., Kinde I., Papadopoulos N., Carpten J.D., Craig D., O'Shaughnessy J., Kinzler K.W., Parmigiani G., Vogelstein B., Diaz L.A., Velculescu V.E. Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing. Sci. Transl. Med. 2012, 4:162ra154.
43. Liu L., Greger J., Shi H., Liu Y., Greshock J., Annan R., Halsey W., Sathe G.M., Martin A.M., Gilmer T.M. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL. Cancer Res. 2009, 69:6871-6878.
44. Madic J., Kiialainen A., Bidard F.C., Birzele F., Ramey G., Leroy Q., Rio Frio T., Vaucher I., Raynal V., Bernard V., Lermine A., Clausen I., Giroud N., Schmucki R., Milder M., Horn C., Spleiss O., Lantz O., Stern M.H., Pierga J.Y., Weisser M., Lebofsky R. Circulating tumor DNA and circulating tumor cells in metastatic triple negative breast cancer patients. Int. J. Cancer 2015, 136:2158-2165.
45. McBride D.J., Orpana A.K., Sotiriou C., Joensuu H., Stephens P.J., Mudie L.J., Hamalainen E., Stebbings L.A., Andersson L.C., Flanagan A.M., Durbecq V., Ignatiadis M., Kallioniemi O., Heckman C.A., Alitalo K., Edgren H., Futreal P.A., Stratton M.R., Campbell P.J. Use of cancer-specific genomic rearrangements to quantify disease burden in plasma from patients with solid tumors. Genes Chromosomes Cancer 2010, 49:1062-1069.
46. McGranahan N., Favero F., de Bruin E.C., Birkbak N.J., Szallasi Z., Swanton C. Clonal status of actionable driver events and the timing of mutational processes in cancer evolution. Sci. Transl. Med. 2015, 7:283ra254.
47. Merenbakh-Lamin K., Ben-Baruch N., Yeheskel A., Dvir A., Soussan-Gutman L., Jeselsohn R., Yelensky R., Brown M., Miller V.A., Sarid D., Rizel S., Klein B., Rubinek T., Wolf I. D538G mutation in estrogen receptor-alpha: a novel mechanism for acquired endocrine resistance in breast cancer. Cancer Res. 2013, 73:6856-6864.
48. Meric-Bernstam F., Brusco L., Shaw K., Horombe C., Kopetz S., Davies M.A., Routbort M., Piha-Paul S.A., Janku F., Ueno N., Hong D., De Groot J., Ravi V., Li Y., Luthra R., Patel K., Broaddus R., Mendelsohn J., Mills G.B. Feasibility of large-scale genomic testing to facilitate enrollment onto genomically matched clinical trials. J. Clin. Oncol. 2015, 33:2753-2762.
49. Mouliere F., Rosenfeld N. Circulating tumor-derived DNA is shorter than somatic DNA in plasma. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:3178-3179.
50. Muller C., Holtschmidt J., Auer M., Heitzer E., Lamszus K., Schulte A., Matschke J., Langer-Freitag S., Gasch C., Stoupiec M., Mauermann O., Peine S., Glatzel M., Speicher M.R., Geigl J.B., Westphal M., Pantel K., Riethdorf S. Hematogenous dissemination of glioblastoma multiforme. Sci. Transl. Med. 2014, 6:247ra101.
51. Murtaza M., Dawson S.J., Pogrebniak K., Rueda O.M., Provenzano E., Grant J., Chin S.F., Tsui D.W., Marass F., Gale D., Ali H.R., Shah P., Contente-Cuomo T., Farahani H., Shumansky K., Kingsbury Z., Humphray S., Bentley D., Shah S.P., Wallis M., Rosenfeld N., Caldas C. Multifocal clonal evolution characterized using circulating tumour DNA in a case of metastatic breast cancer. Nat. Commun. 2015, 6:8760.
52. Murtaza M., Dawson S.J., Tsui D.W., Gale D., Forshew T., Piskorz A.M., Parkinson C., Chin S.F., Kingsbury Z., Wong A.S., Marass F., Humphray S., Hadfield J., Bentley D., Chin T.M., Brenton J.D., Caldas C., Rosenfeld N. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 2013, 497:108-112.
53. Nagalingam A., Tighiouart M., Ryden L., Joseph L., Landberg G., Saxena N.K., Sharma D. Med1 plays a critical role in the development of tamoxifen resistance. Carcinogenesis 2012, 33:918-930.
54. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., Cook K., Stepansky A., Levy D., Esposito D., Muthuswamy L., Krasnitz A., McCombie W.R., Hicks J., Wigler M. Tumour evolution inferred by single-cell sequencing. Nature 2011, 472:90-94.
55. Nik-Zainal S., Van Loo P., Wedge D.C., Alexandrov L.B., Greenman C.D., Lau K.W., Raine K., Jones D., Marshall J., Ramakrishna M., Shlien A., Cooke S.L., Hinton J., Menzies A., Stebbings L.A., Leroy C., Jia M., Rance R., Mudie L.J., Gamble S.J., Stephens P.J., McLaren S., Tarpey P.S., Papaemmanuil E., Davies H.R., Varela I., McBride D.J., Bignell G.R., Leung K., Butler A.P., Teague J.W., Martin S., Jonsson G., Mariani O., Boyault S., Miron P., Fatima A., Langerod A., Aparicio S.A., Tutt A., Sieuwerts A.M., Borg A., Thomas G., Salomon A.V., Richardson A.L., Borresen-Dale A.L., Futreal P.A., Stratton M.R., Campbell P.J. The life history of 21 breast cancers. Cell 2012, 149:994-1007. Breast Cancer Working Group of the International Cancer Genome, C.
56. Olsson E., Winter C., George A., Chen Y., Howlin J., Tang M.H., Dahlgren M., Schulz R., Grabau D., van Westen D., Ferno M., Ingvar C., Rose C., Bendahl P.O., Ryden L., Borg A., Gruvberger-Saal S.K., Jernstrom H., Saal L.H. Serial monitoring of circulating tumor DNA in patients with primary breast cancer for detection of occult metastatic disease. EMBO Mol. Med. 2015, 18:1034-1047.
57. Oshiro C., Kagara N., Naoi Y., Shimoda M., Shimomura A., Maruyama N., Shimazu K., Kim S.J., Noguchi S. PIK3CA mutations in serum DNA are predictive of recurrence in primary breast cancer patients. Breast Cancer Res. Treat 2015, 150:299-307.
58. Pan W., Gu W., Nagpal S., Gephart M.H., Quake S.R. Brain tumor mutations detected in cerebral spinal fluid. Clin. Chem. 2015, 61:514-522.
59. Robinson D.R., Wu Y.M., Vats P., Su F., Lonigro R.J., Cao X., Kalyana-Sundaram S., Wang R., Ning Y., Hodges L., Gursky A., Siddiqui J., Tomlins S.A., Roychowdhury S., Pienta K.J., Kim S.Y., Roberts J.S., Rae J.M., Van Poznak C.H., Hayes D.F., Chugh R., Kunju L.P., Talpaz M., Schott A.F., Chinnaiyan A.M. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat. Genet. 2013, 45:1446-1451.
60. Rothe F., Laes J.F., Lambrechts D., Smeets D., Vincent D., Maetens M., Fumagalli D., Michiels S., Drisis S., Moerman C., Detiffe J.P., Larsimont D., Awada A., Piccart M., Sotiriou C., Ignatiadis M. Plasma circulating tumor DNA as an alternative to metastatic biopsies for mutational analysis in breast cancer. Ann. Oncol. 2014, 25:1959-1965.
61. Schiavon G., Hrebien S., Garcia-Murillas I., Cutts R.J., Pearson A., Tarazona N., Fenwick K., Kozarewa I., Lopez-Knowles E., Ribas R., Nerurkar A., Osin P., Chandarlapaty S., Martin L.A., Dowsett M., Smith I.E., Turner N.C. Analysis of ESR1 mutation in circulating tumor DNA demonstrates evolution during therapy for metastatic breast cancer. Sci. Transl. Med. 2015, 7. 313ra182.
62. Seoane J., De Mattos-Arruda L. Escaping out of the brain. Cancer Discov. 2014, 4:1259-1261.
63. Shah S.P., Morin R.D., Khattra J., Prentice L., Pugh T., Burleigh A., Delaney A., Gelmon K., Guliany R., Senz J., Steidl C., Holt R.A., Jones S., Sun M., Leung G., Moore R., Severson T., Taylor G.A., Teschendorff A.E., Tse K., Turashvili G., Varhol R., Warren R.L., Watson P., Zhao Y., Caldas C., Huntsman D., Hirst M., Marra M.A., Aparicio S. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009, 461:809-813.
64. Shah S.P., Roth A., Goya R., Oloumi A., Ha G., Zhao Y., Turashvili G., Ding J., Tse K., Haffari G., Bashashati A., Prentice L.M., Khattra J., Burleigh A., Yap D., Bernard V., McPherson A., Shumansky K., Crisan A., Giuliany R., Heravi-Moussavi A., Rosner J., Lai D., Birol I., Varhol R., Tam A., Dhalla N., Zeng T., Ma K., Chan S.K., Griffith M., Moradian A., Cheng S.W., Morin G.B., Watson P., Gelmon K., Chia S., Chin S.F., Curtis C., Rueda O.M., Pharoah P.D., Damaraju S., Mackey J., Hoon K., Harkins T., Tadigotla V., Sigaroudinia M., Gascard P., Tlsty T., Costello J.F., Meyer I.M., Eaves C.J., Wasserman W.W., Jones S., Huntsman D., Hirst M., Caldas C., Marra M.A., Aparicio S. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012, 486:395-399.
65. Simon R., Roychowdhury S. Implementing personalized cancer genomics in clinical trials. Nat. Rev. Drug Discov. 2013, 12:358-369.
66. Stephens P.J., Tarpey P.S., Davies H., Van Loo P., Greenman C., Wedge D.C., Nik-Zainal S., Martin S., Varela I., Bignell G.R., Yates L.R., Papaemmanuil E., Beare D., Butler A., Cheverton A., Gamble J., Hinton J., Jia M., Jayakumar A., Jones D., Latimer C., Lau K.W., McLaren S., McBride D.J., Menzies A., Mudie L., Raine K., Rad R., Chapman M.S., Teague J., Easton D., Langerod A., Oslo Breast Cancer, C., Lee M.T., Shen C.Y., Tee B.T., Huimin B.W., Broeks A., Vargas A.C., Turashvili G., Martens J., Fatima A., Miron P., Chin S.F., Thomas G., Boyault S., Mariani O., Lakhani S.R., van de Vijver M., van 't Veer L., Foekens J., Desmedt C., Sotiriou C., Tutt A., Caldas C., Reis-Filho J.S., Aparicio S.A., Salomon A.V., Borresen-Dale A.L., Richardson A.L., Campbell P.J., Futreal P.A., Stratton M.R. The landscape of cancer genes and mutational processes in breast cancer. Nature 2012, 486:400-404.
67. Sullivan J.P., Nahed B.V., Madden M.W., Oliveira S.M., Springer S., Bhere D., Chi A.S., Wakimoto H., Rothenberg S.M., Sequist L.V., Kapur R., Shah K., Iafrate A.J., Curry W.T., Loeffler J.S., Batchelor T.T., Louis D.N., Toner M., Maheswaran S., Haber D.A. Brain tumor cells in circulation are enriched for mesenchymal gene expression. Cancer Discov. 2014, 4:1299-1309.
68. Toy W., Shen Y., Won H., Green B., Sakr R.A., Will M., Li Z., Gala K., Fanning S., King T.A., Hudis C., Chen D., Taran T., Hortobagyi G., Greene G., Berger M., Baselga J., Chandarlapaty S. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat. Genet. 2013, 45:1439-1445.
69. Yates L.R., Gerstung M., Knappskog S., Desmedt C., Gundem G., Van Loo P., Aas T., Alexandrov L.B., Larsimont D., Davies H., Li Y., Ju Y.S., Ramakrishna M., Haugland H.K., Lilleng P.K., Nik-Zainal S., McLaren S., Butler A., Martin S., Glodzik D., Menzies A., Raine K., Hinton J., Jones D., Mudie L.J., Jiang B., Vincent D., Greene-Colozzi A., Adnet P.Y., Fatima A., Maetens M., Ignatiadis M., Stratton M.R., Sotiriou C., Richardson A.L., Lonning P.E., Wedge D.C., Campbell P.J. Subclonal diversification of primary breast cancer revealed by multiregion sequencing. Nat. Med. 2015, 21:751-759.