Clinical Applications of Circulating Tumor DNA in Monitoring Breast Cancer Drug Resistance

References

• Bray F , FerlayJ, SoerjomataramIet al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.68(6), 394–424 (2018).
   PubMed Web of Science ®Google Scholar
• Parikh AR , LeshchinerI, ElaginaLet al. Liquid versus tissue biopsy for detecting acquired resistance and tumor heterogeneity in gastrointestinal cancers. Nat. Med.25(9), 1415–1421 (2019).
   PubMed Web of Science ®Google Scholar
• Corcoran RB , ChabnerBA. Application of cell-free DNA analysis to cancer treatment. N. Engl J. Med.379(18), 1754–1765 (2018).
   PubMed Web of Science ®Google Scholar
• Fernandez-Lazaro D , GarciaHernandez JL, GarciaACet al. Liquid biopsy as novel tool in precision medicine: origins, properties, identification and clinical perspective of cancer’s biomarkers. Diagnostics (Basel)10(4), e215 (2020).
   PubMedGoogle Scholar
• Oliveira KCS , RamosIB, SilvaJMCet al. Current perspectives on circulating tumor DNA, precision medicine, and personalized clinical management of cancer. Mol. Cancer Res.18(4), 517–528 (2020).
   PubMed Web of Science ®Google Scholar
• Mandel P , MetaisP. Les acides nucléiques du plasma sanguin chez l’homme. C R Seances Soc. Biol. Fil.142(3–4), 241–243 (1948).
   PubMedGoogle Scholar
• Leon SA , ShapiroB, SklaroffDMet al. Free DNA in the serum of cancer patients and the effect of therapy. Cancer Res.37(3), 646–650 (1977).
   PubMed Web of Science ®Google Scholar
• Wan JCM , MassieC, Garcia-CorbachoJet al. Liquid biopsies come of age: towards implementation of circulating tumour DNA. Nat. Rev. Cancer17(4), 223–238 (2017).
   PubMed Web of Science ®Google Scholar
• Diehl F , SchmidtK, ChotiMAet al. Circulating mutant DNA to assess tumor dynamics. Nat. Med.14(9), 985–990 (2008).
   PubMed Web of Science ®Google Scholar
• Stahl T , BohmeMU, KrogerNet al. Digital PCR to assess hematopoietic chimerism after allogeneic stem cell transplantation. Exp. Hematol.43(6), 462–468 e461 (2015).
   PubMed Web of Science ®Google Scholar
• Dressman D , YanH, TraversoGet al. Transforming single DNA molecules into fluorescent magnetic particles for detection and enumeration of genetic variations. Proc. Natl Acad. Sci. USA100(15), 8817–8822 (2003).
   PubMed Web of Science ®Google Scholar
• Postel M , RoosenA, Laurent-PuigPet al. Droplet-based digital PCR and next generation sequencing for monitoring circulating tumor DNA: a cancer diagnostic perspective. Expert Rev. Mol. Diagn.18(1), 7–17 (2018).
   PubMed Web of Science ®Google Scholar
• Buono G , GerratanaL, BulfoniMet al. Circulating tumor DNA analysis in breast cancer: is it ready for prime-time? Cancer Treat. Rev. 73, 73–83 (2019).
   PubMed Web of Science ®Google Scholar
• Huang T , ZhugeJ, ZhangWW. Sensitive detection of BRAF V600E mutation by amplification refractory mutation system (ARMS)–PCR. Biomark. Res.1(1), 3 (2013).
   PubMedGoogle Scholar
• Forshew T , MurtazaM, ParkinsonCet al. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci. Transl. Med.4(136), 136ra168 (2012).
   Web of Science ®Google Scholar
• Kinde I , WuJ, PapadopoulosNet al. Detection and quantification of rare mutations with massively parallel sequencing. Proc. Natl Acad. Sci. U S A108(23), 9530–9535 (2011).
   PubMed Web of Science ®Google Scholar
• Newman AM , BratmanSV, ToJet al. An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nat. Med.20(5), 548–554 (2014).
   PubMed Web of Science ®Google Scholar
• Weiser DA , West-SzymanskiDC, FraintEet al. Progress toward liquid biopsies in pediatric solid tumors. Cancer Metastasis Rev.38(4), 553–571 (2019).
   PubMed Web of Science ®Google Scholar
• Koeppel F , BlanchardS, JoveletCet al. Whole exome sequencing for determination of tumor mutation load in liquid biopsy from advanced cancer patients. PLoS ONE12(11), e0188174 (2017).
   PubMed Web of Science ®Google Scholar
• Nakagawa H , WardellCP, FurutaMet al. Cancer whole-genome sequencing: present and future. Oncogene34(49), 5943–5950 (2015).
   PubMed Web of Science ®Google Scholar
• Leary RJ , SausenM, KindeIet al. Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing. Sci. Transl. Med.4(162), 162ra154 (2012).
   PubMed Web of Science ®Google Scholar
• Vendrell JA , Mau-ThemFT, BegantonBet al. Circulating cell free tumor DNA detection as a routine tool for lung cancer patient management. Int. J. Mol. Sci.18(2), 264 (2017).
   PubMed Web of Science ®Google Scholar
• McBride DJ , OrpanaAK, SotiriouCet al. Use of cancer-specific genomic rearrangements to quantify disease burden in plasma from patients with solid tumors. Genes Chromosomes Cancer49(11), 1062–1069 (2010).
   PubMed Web of Science ®Google Scholar
• Leary RJ , KindeI, DiehlFet al. Development of personalized tumor biomarkers using massively parallel sequencing. Sci. Transl. Med.2(20), 20ra14 (2010).
   PubMed Web of Science ®Google Scholar
• Dawson SJ , TsuiDW, MurtazaMet al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl J. Med.368(13), 1199–1209 (2013).
   PubMed Web of Science ®Google Scholar
• Agassi R , CzeigerD, ShakedGet al. Measurement of circulating cell-free DNA levels by a simple fluorescent test in patients with breast cancer. Am. J. Clin. Pathol.143(1), 18–24 (2015).
   PubMed Web of Science ®Google Scholar
• Zhang X , ZhaoW, WeiWet al. Parallel analyses of somatic mutations in plasma circulating tumor DNA (ctDNA) and matched tumor tissues in early-stage breast cancer. Clin. Cancer Res.25(21), 6546–6553 (2019).
   PubMed Web of Science ®Google Scholar
• Garcia-Murillas I , SchiavonG, WeigeltBet al. Mutation tracking in circulating tumor DNA predicts relapse in early breast cancer. Sci. Transl. Med.7(302), 302ra133 (2015).
   PubMed Web of Science ®Google Scholar
• Garcia-Murillas I , ChopraN, Comino-MendezIet al. Assessment of molecular relapse detection in early-stage breast cancer. JAMA Oncol.5(10), 1473–1478 (2019).
   PubMed Web of Science ®Google Scholar
• Parsons HA , RhoadesJ, ReedSCet al. Sensitive detection of minimal residual disease in patients treated for early-stage breast cancer. Clin. Cancer Res.26(11), 2556–2564 (2020).
   PubMed Web of Science ®Google Scholar
• Murtaza M , DawsonSJ, TsuiDWet al. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature497(7447), 108–112 (2013).
   PubMed Web of Science ®Google Scholar
• Emens LA . Breast cancer immunotherapy: facts and hopes. Clin. Cancer Res.24(3), 511–520 (2018).
   PubMed Web of Science ®Google Scholar
• Le DT , DurhamJN, SmithKNet al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science357(6349), 409–413 (2017).
   PubMed Web of Science ®Google Scholar
• Zhao P , LiL, JiangXet al. Mismatch repair deficiency/microsatellite instability–high as a predictor for anti-PD-1/PD-L1 immunotherapy efficacy. J. Hematol. Oncol.12(1), 54 (2019).
   PubMed Web of Science ®Google Scholar
• Chae YK , DavisAA, AgteSet al. Clinical implications of circulating tumor DNA tumor mutational burden (ctDNA TMB) in non-small cell lung cancer. Oncologist24(6), 820–828 (2019).
   PubMed Web of Science ®Google Scholar
• Hellmann MD , NabetBY, RizviHet al. Circulating tumor DNA analysis to assess risk of progression after long-term response to PD-(L)1 blockade in NSCLC. Clin. Cancer Res.26(12), 2849–2858 (2020).
   PubMed Web of Science ®Google Scholar
• Goldberg SB , NarayanA, KoleAJet al. Early assessment of lung cancer immunotherapy response via circulating tumor DNA. Clin. Cancer Res.24(8), 1872–1880 (2018).
   PubMed Web of Science ®Google Scholar
• Peng W , ChenJQ, LiuCet al. Loss of PTEN promotes resistance to T cell–mediated immunotherapy. Cancer Discov.6(2), 202–216 (2016).
   PubMed Web of Science ®Google Scholar
• George S , MiaoD, DemetriGDet al. Loss of PTEN is associated with resistance to anti-PD-1 checkpoint blockade therapy in metastatic uterine leiomyosarcoma. Immunity46(2), 197–204 (2017).
   PubMed Web of Science ®Google Scholar
• Schiavon G , HrebienS, Garcia-MurillasIet al. Analysis of ESR1 mutation in circulating tumor DNA demonstrates evolution during therapy for metastatic breast cancer. Sci. Transl. Med.7(313), 313ra182 (2015).
   PubMed Web of Science ®Google Scholar
• Fribbens C , O’LearyB, KilburnLet al. Plasma ESR1 mutations and the treatment of estrogen receptor–positive advanced breast cancer. J. Clin. Oncol.34(25), 2961–2968 (2016).
   PubMed Web of Science ®Google Scholar
• Chandarlapaty S , ChenD, HeWet al. Prevalence of ESR1 mutations in cell-free DNA and outcomes in metastatic breast cancer: a secondary analysis of the BOLERO-2 clinical trial. JAMA Oncol.2(10), 1310–1315 (2016).
   PubMed Web of Science ®Google Scholar
• Cristofanilli M , DeMicheleA, GiorgettiCet al. Predictors of prolonged benefit from palbociclib plus fulvestrant in women with endocrine-resistant hormone receptor–positive/human epidermal growth factor receptor 2–negative metastatic breast cancer in PALOMA-3. Eur. J. Cancer104, 21–31 (2018).
   PubMed Web of Science ®Google Scholar
• Fribbens C , GarciaMurillas I, BeaneyMet al. Tracking evolution of aromatase inhibitor resistance with circulating tumour DNA analysis in metastatic breast cancer. Ann. Oncol.29(1), 145–153 (2018).
   PubMed Web of Science ®Google Scholar
• O’Leary B , CuttsRJ, LiuYet al. The genetic landscape and clonal evolution of breast cancer resistance to palbociclib plus fulvestrant in the PALOMA-3 trial. Cancer Discov.8(11), 1390–1403 (2018).
   PubMed Web of Science ®Google Scholar
• Board RE , WardleyAM, DixonJMet al. Detection of PIK3CA mutations in circulating free DNA in patients with breast cancer. Breast Cancer Res. Treat.120(2), 461–467 (2010).
   PubMed Web of Science ®Google Scholar
• Takeshita T , YamamotoY, Yamamoto-IbusukiMet al. Prognostic role of PIK3CA mutations of cell-free DNA in early-stage triple negative breast cancer. Cancer Sci.106(11), 1582–1589 (2015).
   PubMed Web of Science ®Google Scholar
• O’Leary B , HrebienS, MordenJPet al. Early circulating tumor DNA dynamics and clonal selection with palbociclib and fulvestrant for breast cancer. Nat. Commun.9(1), 896 (2018).
   PubMedGoogle Scholar
• Moynahan ME , ChenD, HeWet al. Correlation between PIK3CA mutations in cell-free DNA and everolimus efficacy in HR(+), HER2(-) advanced breast cancer: results from BOLERO-2. Br. J. Cancer116(6), 726–730 (2017).
   PubMed Web of Science ®Google Scholar
• Ma F , ZhuW, GuanYet al. ctDNA dynamics: a novel indicator to track resistance in metastatic breast cancer treated with anti-HER2 therapy. Oncotarget7(40), 66020–66031 (2016).
   PubMedGoogle Scholar
• Chen Z , SunT, YangZet al. Monitoring treatment efficacy and resistance in breast cancer patients via circulating tumor DNA genomic profiling. Mol. Genet. Genomic Med.8(2), e1079 (2020).
   PubMed Web of Science ®Google Scholar
• Liggett TE , MelnikovAA, MarksJRet al. Methylation patterns in cell-free plasma DNA reflect removal of the primary tumor and drug treatment of breast cancer patients. Int. J. Cancer128(2), 492–499 (2011).
   PubMed Web of Science ®Google Scholar
• Kajabova V , SmolkovaB, ZmetakovaIet al. RASSF1A promoter methylation levels positively correlate with estrogen receptor expression in breast cancer patients. Transl. Oncol.6(3), 297–304 (2013).
   PubMed Web of Science ®Google Scholar
• Mastoraki S , StratiA, TzanikouEet al. ESR1 methylation: a liquid biopsy–based epigenetic assay for the follow-up of patients with metastatic breast cancer receiving endocrine treatment. Clin. Cancer Res.24(6), 1500–1510 (2018).
   PubMed Web of Science ®Google Scholar
• Zmetakova I , DanihelL, SmolkovaBet al. Evaluation of protein expression and DNA methylation profiles detected by pyrosequencing in invasive breast cancer. Neoplasma60(6), 635–646 (2013).
   PubMed Web of Science ®Google Scholar
• Muller HM , WidschwendterA, FieglHet al. DNA methylation in serum of breast cancer patients: an independent prognostic marker. Cancer Res.63(22), 7641–7645 (2003).
   PubMed Web of Science ®Google Scholar
• Martinez-Galan J , Torres-TorresB, NunezMIet al. ESR1 gene promoter region methylation in free circulating DNA and its correlation with estrogen receptor protein expression in tumor tissue in breast cancer patients. BMC Cancer14, 59 (2014).
   PubMed Web of Science ®Google Scholar
• Fiegl H , MillingerS, Mueller-HolznerEet al. Circulating tumor-specific DNA: a marker for monitoring efficacy of adjuvant therapy in cancer patients. Cancer Res.65(4), 1141–1145 (2005).
   PubMed Web of Science ®Google Scholar
• Takahashi H , KagaraN, TaneiTet al. Correlation of methylated circulating tumor DNA with response to neoadjuvant chemotherapy in breast cancer patients. Clin. Breast Cancer17(1), 61–69.e63 (2017).
   PubMed Web of Science ®Google Scholar
• Sharma G , MirzaS, ParshadRet al. DNA methylation of circulating DNA: a marker for monitoring efficacy of neoadjuvant chemotherapy in breast cancer patients. Tumour Biol. (6), 1837–1843 (2012).
   PubMedGoogle Scholar
• Fujita N , NakayamaT, YamamotoNet al. Methylated DNA and total DNA in serum detected by one-step methylation-specific PCR is predictive of poor prognosis for breast cancer patients. Oncology83(5), 273–282 (2012).
   PubMed Web of Science ®Google Scholar
• Li Z , GuoX, TangLet al. Methylation analysis of plasma cell-free DNA for breast cancer early detection using bisulfite next-generation sequencing. Tumour Biol.37(10), 13111–13119 (2016).
   PubMedGoogle Scholar
• Panagopoulou M , KaraglaniM, BalgkouranidouIet al. Circulating cell-free DNA in breast cancer: size profiling, levels, and methylation patterns lead to prognostic and predictive classifiers. Oncogene38(18), 3387–3401 (2019).
   PubMed Web of Science ®Google Scholar
• van Steenhoven JEC , KuijerA, van DiestPJet al. Conventional pathology versus gene signatures for assessing luminal A and B type breast cancers: results of a prospective cohort study. Genes (Basel)9(5), 261 (2018).
   PubMed Web of Science ®Google Scholar
• Robinson DR , WuYM, VatsPet al. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat. Genet.45(12), 1446–1451 (2013).
   PubMed Web of Science ®Google Scholar
• Jeselsohn R , BuchwalterG, DeAngelis Cet al. ESR1 mutations – a mechanism for acquired endocrine resistance in breast cancer. Nat. Rev. Clin. Oncol.12(10), 573–583 (2015).
   PubMed Web of Science ®Google Scholar
• Samuels Y , VelculescuVE. Oncogenic mutations of PIK3CA in human cancers. Cell Cycle3(10), 1221–1224 (2004).
   PubMed Web of Science ®Google Scholar
• Ellis MJ , LinL, CrowderRet al. Phosphatidyl-inositol-3-kinase alpha catalytic subunit mutation and response to neoadjuvant endocrine therapy for estrogen receptor positive breast cancer. Breast Cancer Res. Treat.119(2), 379–390 (2010).
   PubMed Web of Science ®Google Scholar
• Wang DS , LiuZX, LuYXet al. Liquid biopsies to track trastuzumab resistance in metastatic HER2-positive gastric cancer. Gut68(7), 1152–1161 (2019).
   PubMed Web of Science ®Google Scholar
• Ramirez-Ardila DE , HelmijrJC, LookMPet al. Hotspot mutations in PIK3CA associate with first-line treatment outcome for aromatase inhibitors but not for tamoxifen. Breast Cancer Res. Treat.139(1), 39–49 (2013).
   PubMed Web of Science ®Google Scholar
• Baselga J , ImSA, IwataHet al. Buparlisib plus fulvestrant versus placebo plus fulvestrant in postmenopausal, hormone receptor–positive, HER2-negative, advanced breast cancer (BELLE-2): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol.18(7), 904–916 (2017).
   PubMed Web of Science ®Google Scholar
• Di Leo A , JohnstonS, LeeKSet al. Buparlisib plus fulvestrant in postmenopausal women with hormone-receptor-positive, HER2-negative, advanced breast cancer progressing on or after mTOR inhibition (BELLE-3): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol.19(1), 87–100 (2018).
   PubMed Web of Science ®Google Scholar
• Andre F , CiruelosE, RubovszkyGet al. Alpelisib for PIK3CA-mutated, hormone receptor–positive advanced breast cancer. N. Engl J. Med.380(20), 1929–1940 (2019).
   PubMed Web of Science ®Google Scholar
• Markham A . Alpelisib: first global approval. Drugs79(11), 1249–1253 (2019).
   PubMed Web of Science ®Google Scholar
• Curtis C , ShahSP, ChinSFet al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature486(7403), 346–352 (2012).
   PubMed Web of Science ®Google Scholar
• Ciriello G , MillerML, AksoyBAet al. Emerging landscape of oncogenic signatures across human cancers. Nat. Genet.45(10), 1127–1133 (2013).
   PubMed Web of Science ®Google Scholar
• Yang X , ZhangK, ZhangCet al. Accuracy of analysis of cfDNA for detection of single nucleotide variants and copy number variants in breast cancer. BMC Cancer19(1), 465 (2019).
   PubMedGoogle Scholar
• Nebbioso A , TambaroFP, Dell’AversanaCet al. Cancer epigenetics: moving forward. PLoS Genet.14(6), e1007362 (2018).
   PubMed Web of Science ®Google Scholar
• Kang G , ChenK, YangFet al. Monitoring of circulating tumor DNA and its aberrant methylation in the surveillance of surgical lung cancer patients: protocol for a prospective observational study. BMC Cancer19(1), 579 (2019).
   PubMedGoogle Scholar
• Li Z , GuoX, WuYet al. Methylation profiling of 48 candidate genes in tumor and matched normal tissues from breast cancer patients. Breast Cancer Res. Treat.149(3), 767–779 (2015).
   PubMed Web of Science ®Google Scholar
• Alix-Panabieres C , PantelK. Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov.6(5), 479–491 (2016).
   PubMed Web of Science ®Google Scholar
• Li J , HanX, YuXet al. Clinical applications of liquid biopsy as prognostic and predictive biomarkers in hepatocellular carcinoma: circulating tumor cells and circulating tumor DNA. J. Exp. Clin. Cancer Res.37(1), 213 (2018).
   PubMedGoogle Scholar
• Cristofanilli M , BuddGT, EllisMJet al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl J. Med.351(8), 781–791 (2004).
   PubMed Web of Science ®Google Scholar
• Deutsch TM , RiethdorfS, FremdCet al. HER2-targeted therapy influences CTC status in metastatic breast cancer. Breast Cancer Res. Treat.182(1), 127–136 (2020).
   Web of Science ®Google Scholar
• Deutsch TM , StefanovicS, FeisstMet al. Cut-off analysis of CTC change under systemic therapy for defining early therapy response in metastatic breast cancer. Cancers12(4), 1055 (2020).
   PubMed Web of Science ®Google Scholar
• Lv Q , GongL, ZhangTet al. Prognostic value of circulating tumor cells in metastatic breast cancer: a systemic review and meta-analysis. Clin. Transl. Oncol.18(3), 322–330 (2016).
   PubMed Web of Science ®Google Scholar
• D’Oronzo S , LoveroD, PalmirottaRet al. Dissection of major cancer gene variants in subsets of circulating tumor cells in advanced breast cancer. Sci. Rep.9(1), 17276 (2019).
   PubMedGoogle Scholar
• Wang C , MuZ, YeZet al. Prognostic value of HER2 status on circulating tumor cells in advanced-stage breast cancer patients with HER2-negative tumors. Breast Cancer Res. Treat.181(3), 679–689 (2020).
   PubMed Web of Science ®Google Scholar
• Beije N , SieuwertsAM, KraanJet al. Estrogen receptor mutations and splice variants determined in liquid biopsies from metastatic breast cancer patients. Mol. Oncol.12(1), 48–57 (2018).
   PubMed Web of Science ®Google Scholar
• Li H , LiuJ, ChenJet al. A serum microRNA signature predicts trastuzumab benefit in HER2-positive metastatic breast cancer patients. Nat. Commun.9(1), 1614 (2018).
   PubMedGoogle Scholar
• Mazel M , JacotW, PantelKet al. Frequent expression of PD-L1 on circulating breast cancer cells. Mol. Oncol.9(9), 1773–1782 (2015).
   PubMed Web of Science ®Google Scholar
• Papadaki MA , KoutsopoulosAV, TsoulfasPGet al. Clinical relevance of immune checkpoints on circulating tumor cells in breast cancer. Cancers (Basel)12(2), 376 (2020).
   PubMed Web of Science ®Google Scholar
• Hrebien S , CitiV, Garcia-MurillasIet al. Early ctDNA dynamics as a surrogate for progression-free survival in advanced breast cancer in the BEECH trial. Ann. Oncol.30(6), 945–952 (2019).
   PubMed Web of Science ®Google Scholar
• Rothwell DG , AyubM, CookNet al. Utility of ctDNA to support patient selection for early phase clinical trials: the TARGET study. Nat. Med.25(5), 738–743 (2019).
   PubMed Web of Science ®Google Scholar
• Clinical trials . Available from: https://clinicaltrials.gov/
   Google Scholar
• Grolz D , HauchS, SchlumpbergerMet al. Liquid biopsy preservation solutions for standardized pre-analytical workflows—venous whole blood and plasma. Curr. Pathobiol. Rep.6(4), 275–286 (2018).
   PubMedGoogle Scholar
• Ghini V , QuaglioD, LuchinatCet al. NMR for sample quality assessment in metabolomics. N. Biotechnol.52, 25–34 (2019).
   PubMed Web of Science ®Google Scholar
• Condorelli R , SpringL, O’ShaughnessyJet al. Polyclonal RB1 mutations and acquired resistance to CDK 4/6 inhibitors in patients with metastatic breast cancer. Ann. Oncol.29(3), 640–645 (2018).
   PubMed Web of Science ®Google Scholar
• Formisano L , LuY, ServettoAet al. Aberrant FGFR signaling mediates resistance to CDK4/6 inhibitors in ER+ breast cancer. Nat. Commun.10(1), 1373 (2019).
   PubMedGoogle Scholar