Cell-free DNA as a molecular tool for monitoring disease progression and response to therapy in breast cancer patients

Breast Cancer Research and Treatment

Volumn 155, Issue 1, 2016, Pages 139-149

  Liang, Diana H ^a   Ensor, Joe E ^a,b   Liu, Zhe bin ^a,c   Patel, Asmita ^b   Patel, Tejal A ^b   Chang, Jenny C ^b   Rodriguez, Angel A ^b  

^a HOUSTON METHODIST HOSPITAL   (United States)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^c FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

Author keywords

Breast cancer; Cell free DNA; Clinical markers

Indexed keywords

CELL FREE DNA; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR 2; LAPATINIB; PACLITAXEL; PERTUZUMAB; PROTEIN P53; TRASTUZUMAB; TRASTUZUMAB EMTANSINE; TUMOR DNA; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ERBB2 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PIK3CA PROTEIN, HUMAN; TUMOR MARKER;

ADULT; ARTICLE; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER EPIDEMIOLOGY; CANCER GROWTH; CANCER INCIDENCE; CANCER STAGING; CANCER SURVIVAL; COPY NUMBER VARIATION; DNA DETERMINATION; EGFR GENE; ERBB2 GENE; FEMALE; GENE; GENE FREQUENCY; GENE MUTATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PIK3CA GENE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SINGLE NUCLEOTIDE POLYMORPHISM; SURVIVAL TIME; TP53 GENE; TREATMENT RESPONSE; AGED; ALLELE; BLOOD; BREAST NEOPLASMS; DISEASE COURSE; GENE AMPLIFICATION; GENETIC VARIATION; GENETICS; METABOLISM; MORTALITY; MUTATION; PATHOLOGY; PROGNOSIS; RETROSPECTIVE STUDY; TREATMENT OUTCOME;

ADULT; AGED; ALLELES; BIOMARKERS, TUMOR; BREAST NEOPLASMS; DISEASE PROGRESSION; DNA COPY NUMBER VARIATIONS; DNA, NEOPLASM; FEMALE; GENE AMPLIFICATION; GENE FREQUENCY; GENETIC VARIATION; HUMANS; MALE; MIDDLE AGED; MUTATION; NEOPLASM STAGING; PHOSPHATIDYLINOSITOL 3-KINASES; POLYMORPHISM, SINGLE NUCLEOTIDE; PROGNOSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RETROSPECTIVE STUDIES; TREATMENT OUTCOME; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84953359146     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-015-3635-5     Document Type: Article

References (41)

1. Meyerson M, Gabriel S, Getz G (2010) Advances in understanding cancer genomes through second-generation sequencing. Nat Rev Genet 11:685–696. doi:10.1038/nrg2841
2. Sato F, Saji S, Toi M (2015) Genomic tumor evolution of breast cancer. Breast Cancer. doi:10.1007/s12282-015-0617-8
3. Bourdeanu L, Luu T (2014) Targeted therapies in breast cancer: implications for advanced oncology practice. J Adv Pract Oncol 5:246–260
4. Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, Bartlett BR, Wang H, Luber B, Alani RM, Antonarakis ES, Azad NS, Bardelli A, Brem H, Cameron JL, Lee CC, Fecher LA, Gallia GL, Gibbs P, Le D, Giuntoli RL, Goggins M, Hogarty MD, Holdhoff M, Hong SM, Jiao Y, Juhl HH, Kim JJ, Siravegna G, Laheru DA, Lauricella C, Lim M, Lipson EJ, Marie SK, Netto GJ, Oliner KS, Olivi A, Olsson L, Riggins GJ, Sartore-Bianchi A, Schmidt K, Shih l M, Oba-Shinjo SM, Siena S, Theodorescu D, Tie J, Harkins TT, Veronese S, Wang TL, Weingart JD, Wolfgang CL, Wood LD, Xing D, Hruban RH, Wu J, Allen PJ, Schmidt CM, Choti MA, Velculescu VE, Kinzler KW, Vogelstein B, Papadopoulos N, Diaz LA, Jr. (2014) Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 6:224ra224. doi: 10.1126/scitranslmed.3007094
5. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, Tarpey P, Varela I, Phillimore B, Begum S, McDonald NQ, Butler A, Jones D, Raine K, Latimer C, Santos CR, Nohadani M, Eklund AC, Spencer-Dene B, Clark G, Pickering L, Stamp G, Gore M, Szallasi Z, Downward J, Futreal PA, Swanton C (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366:883–892. doi:10.1056/NEJMoa1113205
6. Wang Y, Waters J, Leung ML, Unruh A, Roh W, Shi X, Chen K, Scheet P, Vattathil S, Liang H, Multani A, Zhang H, Zhao R, Michor F, Meric-Bernstam F, Navin NE (2014) Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 512:155–160. doi:10.1038/nature13600
7. 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 WR, Hicks J, Wigler M (2011) Tumour evolution inferred by single-cell sequencing. Nature 472:90–94. doi:10.1038/nature09807
8. Zardavas D, Irrthum A, Swanton C, Piccart M (2015) Clinical management of breast cancer heterogeneity. Nat Rev Clin Oncol 12:381–394. doi:10.1038/nrclinonc.2015.73
9. Bedard PL, Hansen AR, Ratain MJ, Siu LL (2013) Tumour heterogeneity in the clinic. Nature 501:355–364. doi:10.1038/nature12627
10. Diaz LA Jr, Williams RT, Wu J, Kinde I, Hecht JR, Berlin J, Allen B, Bozic I, Reiter JG, Nowak MA, Kinzler KW, Oliner KS, Vogelstein B (2012) The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486:537–540. doi:10.1038/nature11219
11. Ma QC, Ennis CA, Aparicio S (2012) Opening Pandora’s Box–the new biology of driver mutations and clonal evolution in cancer as revealed by next generation sequencing. Curr Opin Genet Dev 22:3–9. doi:10.1016/j.gde.2012.01.008
12. Dawson SJ, Tsui DW, Murtaza M, Biggs H, Rueda OM, Chin SF, Dunning MJ, Gale D, Forshew T, Mahler-Araujo B, Rajan S, Humphray S, Becq J, Halsall D, Wallis M, Bentley D, Caldas C, Rosenfeld N (2013) Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med 368:1199–1209. doi:10.1056/NEJMoa1213261
13. Schwarzenbach H (2013) Circulating nucleic acids as biomarkers in breast cancer. Breast Cancer Res 15:211. doi:10.1186/bcr3446
14. Leon SA, Shapiro B, Sklaroff DM, Yaros MJ (1977) Free DNA in the serum of cancer patients and the effect of therapy. Cancer Res 37:646–650
15. Stroun M, Anker P, Maurice P, Lyautey J, Lederrey C, Beljanski M (1989) Neoplastic characteristics of the DNA found in the plasma of cancer patients. Oncology 46:318–322
16. Kohler C, Radpour R, Barekati Z, Asadollahi R, Bitzer J, Wight E, Burki N, Diesch C, Holzgreve W, Zhong XY (2009) Levels of plasma circulating cell free nuclear and mitochondrial DNA as potential biomarkers for breast tumors. Mol Cancer 8:105. doi:10.1186/1476-4598-8-105
17. Olsson E, Winter C, George A, Chen Y, Howlin J, Tang MH, Dahlgren M, Schulz R, Grabau D, van Westen D, Ferno M, Ingvar C, Rose C, Bendahl PO, Ryden L, Borg A, Gruvberger-Saal SK, Jernstrom H, Saal LH (2015) Serial monitoring of circulating tumor DNA in patients with primary breast cancer for detection of occult metastatic disease. EMBO Mol Med 7:1034–1047. doi:10.15252/emmm.201404913
18. Lanman RB, Mortimer SA, Zill OA, Sebisanovic D, Lopez R, Blau S, Collisson EA, Divers SG, Hoon DS, Kopetz ES, Lee J, Nikolinakos PG, Baca AM, Kermani BG, Eltoukhy H, Talasaz A (2015) Analytical and clinical validation of a digital sequencing panel for quantitative, highly accurate evaluation of cell-free circulating tumor DNA. PLoS ONE 10:e0140712. doi:10.1371/journal.pone.0140712
19. Shah M, Denlinger CS (2015) Optimal post-treatment surveillance in cancer survivors: is more really better? Oncology (Williston Park) 29:230–240
20. Shaw JA, Stebbing J (2014) Circulating free DNA in the management of breast cancer. Ann Transl Med 2:3. doi:10.3978/j.issn.2305-5839.2013.06.06
21. Smerage JB, Barlow WE, Hortobagyi GN, Winer EP, Leyland-Jones B, Srkalovic G, Tejwani S, Schott AF, O’Rourke MA, Lew DL, Doyle GV, Gralow JR, Livingston RB, Hayes DF (2014) Circulating tumor cells and response to chemotherapy in metastatic breast cancer: SWOG S0500. J Clin Oncol 32:3483–3489. doi:10.1200/JCO.2014.56.2561
22. Rothe F, Laes JF, Lambrechts D, Smeets D, Vincent D, Maetens M, Fumagalli D, Michiels S, Drisis S, Moerman C, Detiffe JP, Larsimont D, Awada A, Piccart M, Sotiriou C, Ignatiadis M (2014) Plasma circulating tumor DNA as an alternative to metastatic biopsies for mutational analysis in breast cancer. Ann Oncol 25:1959–1965. doi:10.1093/annonc/mdu288
23. Huang ZH, Li LH, Hua D (2006) Quantitative analysis of plasma circulating DNA at diagnosis and during follow-up of breast cancer patients. Cancer Lett 243:64–70. doi:10.1016/j.canlet.2005.11.027
24. Higgins MJ, Jelovac D, Barnathan E, Blair B, Slater S, Powers P, Zorzi J, Jeter SC, Oliver GR, Fetting J, Emens L, Riley C, Stearns V, Diehl F, Angenendt P, Huang P, Cope L, Argani P, Murphy KM, Bachman KE, Greshock J, Wolff AC, Park BH (2012) Detection of tumor PIK3CA status in metastatic breast cancer using peripheral blood. Clin Cancer Res 18:3462–3469. doi:10.1158/1078-0432.CCR-11-2696
25. Board RE, Wardley AM, Dixon JM, Armstrong AC, Howell S, Renshaw L, Donald E, Greystoke A, Ranson M, Hughes A, Dive C (2010) Detection of PIK3CA mutations in circulating free DNA in patients with breast cancer. Breast Cancer Res Treat 120:461–467. doi:10.1007/s10549-010-0747-9
26. Leiserson MD, Blokh D, Sharan R, Raphael BJ (2013) Simultaneous identification of multiple driver pathways in cancer. PLoS Comput Biol 9:e1003054. doi:10.1371/journal.pcbi.1003054
27. Gustin JP, Cosgrove DP, Park BH (2008) The PIK3CA gene as a mutated target for cancer therapy. Curr Cancer Drug Targets 8:733–740
28. Ahn T, Park T (2014) Pathway-driven discovery of rare mutational impact on cancer. Biomed Res Int 2014:171892. doi:10.1155/2014/171892
29. Mayer IA, Arteaga CL (2014) PIK3CA activating mutations: a discordant role in early versus advanced hormone-dependent estrogen receptor-positive breast cancer? J Clin Oncol 32:2932–2934. doi:10.1200/JCO.2014.55.9591
30. Loi S, Haibe-Kains B, Majjaj S, Lallemand F, Durbecq V, Larsimont D, Gonzalez-Angulo AM, Pusztai L, Symmans WF, Bardelli A, Ellis P, Tutt AN, Gillett CE, Hennessy BT, Mills GB, Phillips WA, Piccart MJ, Speed TP, McArthur GA, Sotiriou C (2010) PIK3CA mutations associated with gene signature of low mTORC1 signaling and better outcomes in estrogen receptor-positive breast cancer. Proc Natl Acad Sci USA 107:10208–10213. doi:10.1073/pnas.0907011107
31. Kalinsky K, Jacks LM, Heguy A, Patil S, Drobnjak M, Bhanot UK, Hedvat CV, Traina TA, Solit D, Gerald W, Moynahan ME (2009) PIK3CA mutation associates with improved outcome in breast cancer. Clin Cancer Res 15:5049–5059. doi:10.1158/1078-0432.CCR-09-0632
32. Kroigard AB, Larsen MJ, Laenkholm AV, Knoop AS, Jensen JD, Bak M, Mollenhauer J, Kruse TA, Thomassen M (2015) Clonal expansion and linear genome evolution through breast cancer progression from pre-invasive stages to asynchronous metastasis. Oncotarget 6:5634–5649
33. Pestrin M, Salvianti F, Galardi F, De Luca F, Turner N, Malorni L, Pazzagli M, Di Leo A, Pinzani P (2015) Heterogeneity of PIK3CA mutational status at the single cell level in circulating tumor cells from metastatic breast cancer patients. Mol Oncol 9:749–757. doi:10.1016/j.molonc.2014.12.001
34. Deng G, Krishnakumar S, Powell AA, Zhang H, Mindrinos MN, Telli ML, Davis RW, Jeffrey SS (2014) Single cell mutational analysis of PIK3CA in circulating tumor cells and metastases in breast cancer reveals heterogeneity, discordance, and mutation persistence in cultured disseminated tumor cells from bone marrow. BMC Cancer 14:456. doi:10.1186/1471-2407-14-456
35. Maxwell KN S-ED, Carpenter EL, Troxel AB, Colameco C, Clark C, et al. (2015) Comparison of mutational spectra in metastatic tumors and cell-free DNA in breast cancer patients. Cancer Res. 75 (15 Supp): Abstract nr618
36. Oshiro C, Kagara N, Naoi Y, Shimoda M, Shimomura A, Maruyama N, Shimazu K, Kim SJ, Noguchi S (2015) PIK3CA mutations in serum DNA are predictive of recurrence in primary breast cancer patients. Breast Cancer Res Treat 150:299–307. doi:10.1007/s10549-015-3322-6
37. Murtaza M, Dawson SJ, Tsui DW, Gale D, Forshew T, Piskorz AM, Parkinson C, Chin SF, Kingsbury Z, Wong AS, Marass F, Humphray S, Hadfield J, Bentley D, Chin TM, Brenton JD, Caldas C, Rosenfeld N (2013) Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 497:108–112. doi:10.1038/nature12065
38. Sefrioui D, Perdrix A, Sarafan-Vasseur N, Dolfus C, Dujon A, Picquenot JM, Delacour J, Cornic M, Bohers E, Leheurteur M, Rigal O, Tennevet I, Thery JC, Alexandru C, Guillemet C, Moldovan C, Veyret C, Frebourg T, Di Fiore F, Clatot F (2015) Short report: monitoring ESR1 mutations by circulating tumor DNA in aromatase inhibitor resistant metastatic breast cancer. Int J Cancer 137:2513–2519. doi:10.1002/ijc.29612
39. Guttery DS, Page K, Hills A, Woodley L, Marchese SD, Rghebi B, Hastings RK, Luo J, Pringle JH, Stebbing J, Coombes RC, Ali S, Shaw JA (2015) Noninvasive detection of activating estrogen receptor 1 (ESR1) mutations in estrogen receptor-positive metastatic breast cancer. Clin Chem 61:974–982. doi:10.1373/clinchem.2015.238717
40. Madic J, Kiialainen A, Bidard FC, 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 MH, Pierga JY, Weisser M, Lebofsky R (2015) Circulating tumor DNA and circulating tumor cells in metastatic triple negative breast cancer patients. Int J Cancer 136:2158–2165. doi:10.1002/ijc.29265
41. Van Poznak C, Somerfield MR, Bast RC, Cristofanilli M, Goetz MP, Gonzalez-Angulo AM, Hicks DG, Hill EG, Liu MC, Lucas W, Mayer IA, Mennel RG, Symmans WF, Hayes DF, Harris LN (2015) Use of Biomarkers to Guide Decisions on Systemic Therapy for Women With Metastatic Breast Cancer: American Society of Clinical Oncology Clinical Practice Guideline. J Clin Oncol 33:2695–2704. doi:10.1200/JCO.2015.61.1459