Journal Article
. 2018 Apr; 173(4):879-893.e13.
doi: 10.1016/j.cell.2018.03.041.

Chemoresistance Evolution in Triple-Negative Breast Cancer Delineated by Single-Cell Sequencing

Charissa Kim 1 Ruli Gao 2 Emi Sei 2 Rachel Brandt 2 Johan Hartman 3 Thomas Hatschek 3 Nicola Crosetto 4 Theodoros Foukakis 5 Nicholas E Navin 6 
Affiliations
  • PMID: 29681456
  •     82 References
  •     180 citations

Abstract

Triple-negative breast cancer (TNBC) is an aggressive subtype that frequently develops resistance to chemotherapy. An unresolved question is whether resistance is caused by the selection of rare pre-existing clones or alternatively through the acquisition of new genomic aberrations. To investigate this question, we applied single-cell DNA and RNA sequencing in addition to bulk exome sequencing to profile longitudinal samples from 20 TNBC patients during neoadjuvant chemotherapy (NAC). Deep-exome sequencing identified 10 patients in which NAC led to clonal extinction and 10 patients in which clones persisted after treatment. In 8 patients, we performed a more detailed study using single-cell DNA sequencing to analyze 900 cells and single-cell RNA sequencing to analyze 6,862 cells. Our data showed that resistant genotypes were pre-existing and adaptively selected by NAC, while transcriptional profiles were acquired by reprogramming in response to chemotherapy in TNBC patients.

Keywords: breast cancer genomics; cancer aneuploidy; chemotherapy; copy-number evolution; intratumor heterogeneity; single-cell sequencing; therapy resistance; triple-negative breast cancer; tumor evolution.

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Mitotic slippage: an old tale with a new twist.
Debottam Sinha, Pascal H G Duijf, Kum Kum Khanna.
Cell Cycle, 2019 Jan 03; 18(1). PMID: 30601084    Free PMC article.
Review.
Insights into Molecular Classifications of Triple-Negative Breast Cancer: Improving Patient Selection for Treatment.
Ana C Garrido-Castro, Nancy U Lin, Kornelia Polyak.
Cancer Discov, 2019 Jan 27; 9(2). PMID: 30679171    Free PMC article.
Highly Cited. Review.
Clonal replacement and heterogeneity in breast tumors treated with neoadjuvant HER2-targeted therapy.
Jennifer L Caswell-Jin, Katherine McNamara, +17 authors, Christina Curtis.
Nat Commun, 2019 Feb 10; 10(1). PMID: 30737380    Free PMC article.
Barcoding reveals complex clonal behavior in patient-derived xenografts of metastatic triple negative breast cancer.
D Merino, T S Weber, +15 authors, S H Naik.
Nat Commun, 2019 Feb 17; 10(1). PMID: 30770823    Free PMC article.
Highly Cited.
Translating insights into tumor evolution to clinical practice: promises and challenges.
Matthew W Fittall, Peter Van Loo.
Genome Med, 2019 Mar 31; 11(1). PMID: 30925887    Free PMC article.
Review.
Dual TGFβ/BMP Pathway Inhibition Enables Expansion and Characterization of Multiple Epithelial Cell Types of the Normal and Cancerous Breast.
Mayuri Prasad, Brijesh Kumar, +5 authors, Harikrishna Nakshatri.
Mol Cancer Res, 2019 Apr 18; 17(7). PMID: 30992305    Free PMC article.
Resistance to neoadjuvant chemotherapy in triple-negative breast cancer mediated by a reversible drug-tolerant state.
Gloria V Echeverria, Zhongqi Ge, +27 authors, Helen Piwnica-Worms.
Sci Transl Med, 2019 Apr 19; 11(488). PMID: 30996079    Free PMC article.
Highly Cited.
Targeting enhancer switching overcomes non-genetic drug resistance in acute myeloid leukaemia.
Charles C Bell, Katie A Fennell, +33 authors, Mark A Dawson.
Nat Commun, 2019 Jun 22; 10(1). PMID: 31222014    Free PMC article.
Profiling molecular regulators of recurrence in chemorefractory triple-negative breast cancers.
Bradley A Hancock, Yu-Hsiang Chen, +14 authors, Milan Radovich.
Breast Cancer Res, 2019 Aug 07; 21(1). PMID: 31383035    Free PMC article.
A general approach for detecting expressed mutations in AML cells using single cell RNA-sequencing.
Allegra A Petti, Stephen R Williams, +7 authors, Timothy J Ley.
Nat Commun, 2019 Aug 16; 10(1). PMID: 31413257    Free PMC article.
Single-cell transcriptomics reveals multi-step adaptations to endocrine therapy.
Sung Pil Hong, Thalia E Chan, +9 authors, Luca Magnani.
Nat Commun, 2019 Sep 04; 10(1). PMID: 31477698    Free PMC article.
Acquisition of chromosome instability is a mechanism to evade oncogene addiction.
Lorena Salgueiro, Christopher Buccitelli, +4 authors, Rocio Sotillo.
EMBO Mol Med, 2020 Feb 08; 12(3). PMID: 32030896    Free PMC article.
Improved detection of differentially represented DNA barcodes for high-throughput clonal phenomics.
Yevhen Akimov, Daria Bulanova, +2 authors, Tero Aittokallio.
Mol Syst Biol, 2020 Mar 19; 16(3). PMID: 32187448    Free PMC article.
Dihydroartemisinin-Loaded Magnetic Nanoparticles for Enhanced Chemodynamic Therapy.
Shengdi Guo, Xianxian Yao, +5 authors, Wuli Yang.
Front Pharmacol, 2020 Mar 27; 11. PMID: 32210814    Free PMC article.
Joint single cell DNA-seq and RNA-seq of gastric cancer cell lines reveals rules of in vitro evolution.
Noemi Andor, Billy T Lau, +9 authors, Hanlee P Ji.
NAR Genom Bioinform, 2020 Mar 28; 2(2). PMID: 32215369    Free PMC article.
Intratumoral Heterogeneity: More Than Just Mutations.
Kunihiko Hinohara, Kornelia Polyak.
Trends Cell Biol, 2019 Apr 17; 29(7). PMID: 30987806    Free PMC article.
Highly Cited. Review.
Relapse-Fated Latent Diagnosis Subclones in Acute B Lineage Leukemia Are Drug Tolerant and Possess Distinct Metabolic Programs.
Stephanie M Dobson, Laura García-Prat, +30 authors, John E Dick.
Cancer Discov, 2020 Feb 23; 10(4). PMID: 32086311    Free PMC article.
Dietary Compound Isoliquiritigenin, an Antioxidant from Licorice, Suppresses Triple-Negative Breast Tumor Growth via Apoptotic Death Program Activation in Cell and Xenograft Animal Models.
Po-Han Lin, Yi-Fen Chiang, +8 authors, Shih-Min Hsia.
Antioxidants (Basel), 2020 Mar 14; 9(3). PMID: 32164337    Free PMC article.
CancerTracer: a curated database for intrapatient tumor heterogeneity.
Chen Wang, Jian Yang, +6 authors, Haoyang Cai.
Nucleic Acids Res, 2019 Nov 09; 48(D1). PMID: 31701131    Free PMC article.
Breast Cancer: A Molecularly Heterogenous Disease Needing Subtype-Specific Treatments.
Ugo Testa, Germana Castelli, Elvira Pelosi.
Med Sci (Basel), 2020 Mar 27; 8(1). PMID: 32210163    Free PMC article.
Review.
Chemotherapy, host response and molecular dynamics in periampullary cancer: the CHAMP study.
Sofie Olsson Hau, Alexandra Petersson, +8 authors, Karin Jirström.
BMC Cancer, 2020 Apr 16; 20(1). PMID: 32293352    Free PMC article.
From Summary Statistics to Gene Trees: Methods for Inferring Positive Selection.
Hussein A Hejase, Noah Dukler, Adam Siepel.
Trends Genet, 2020 Jan 20; 36(4). PMID: 31954511    Free PMC article.
Review.
Modeling Basins of Attraction for Breast Cancer Using Hopfield Networks.
Alessandra Jordano Conforte, Leon Alves, +2 authors, Fabrício Alves Barbosa da Silva.
Front Genet, 2020 Apr 23; 11. PMID: 32318098    Free PMC article.
Single‑cell RNA sequencing of t(8;21) acute myeloid leukemia for risk prediction.
Qian Xiong, Sai Huang, +12 authors, Li Yu.
Oncol Rep, 2020 Apr 24; 43(4). PMID: 32323795    Free PMC article.
RNA-sequencing and microarray data mining revealing: the aberrantly expressed mRNAs were related with a poor outcome in the triple negative breast cancer patients.
Hongjun Fei, Songchang Chen, Chenming Xu.
Ann Transl Med, 2020 May 02; 8(6). PMID: 32355807    Free PMC article.
New Insights Into the Role of Phenotypic Plasticity and EMT in Driving Cancer Progression.
Sugandha Bhatia, Peiyu Wang, Alan Toh, Erik W Thompson.
Front Mol Biosci, 2020 May 12; 7. PMID: 32391381    Free PMC article.
Review.
Cellular Plasticity in Breast Cancer Progression and Therapy.
Deguang Kong, Connor J Hughes, Heide L Ford.
Front Mol Biosci, 2020 May 12; 7. PMID: 32391382    Free PMC article.
Review.
Chemotherapy use near the end-of-life in patients with metastatic breast cancer.
Luisa Edman Kessler, Johnny Sigfridsson, +4 authors, Alexios Matikas.
Breast Cancer Res Treat, 2020 May 10; 181(3). PMID: 32383058    Free PMC article.
Resistance to targeted therapies as a multifactorial, gradual adaptation to inhibitor specific selective pressures.
Robert Vander Velde, Nara Yoon, +15 authors, Andriy Marusyk.
Nat Commun, 2020 May 16; 11(1). PMID: 32409712    Free PMC article.
The Landscape of Targeted Therapies in TNBC.
Elena Vagia, Devalingam Mahalingam, Massimo Cristofanilli.
Cancers (Basel), 2020 Apr 12; 12(4). PMID: 32276534    Free PMC article.
Review.
SCOPE: A Normalization and Copy-Number Estimation Method for Single-Cell DNA Sequencing.
Rujin Wang, Dan-Yu Lin, Yuchao Jiang.
Cell Syst, 2020 May 22; 10(5). PMID: 32437686    Free PMC article.
Hypoxia-Driven Immune Escape in the Tumor Microenvironment.
Alyssa Vito, Nader El-Sayes, Karen Mossman.
Cells, 2020 Apr 23; 9(4). PMID: 32316260    Free PMC article.
Review.
Humanin Promotes Tumor Progression in Experimental Triple Negative Breast Cancer.
Mariela A Moreno Ayala, María Florencia Gottardo, +9 authors, Marianela Candolfi.
Sci Rep, 2020 May 24; 10(1). PMID: 32444831    Free PMC article.
Unmet Clinical Need: Developing Prognostic Biomarkers and Precision Medicine to Forecast Early Tumor Relapse, Detect Chemo-Resistance and Improve Overall Survival in High-Risk Breast Cancer.
Gagan Gupta, Caroline Dasom Lee, +10 authors, Amy H Tang.
Ann Breast Cancer Ther, 2020 Jun 17; 4(1). PMID: 32542231    Free PMC article.
Induction of DNMT3B by PGE2 and IL6 at Distant Metastatic Sites Promotes Epigenetic Modification and Breast Cancer Colonization.
Jae Young So, Nicolas Skrypek, +14 authors, Li Yang.
Cancer Res, 2020 Apr 09; 80(12). PMID: 32265226    Free PMC article.
Identifying Therapies to Combat Epithelial Mesenchymal Plasticity-Associated Chemoresistance to Conventional Breast Cancer Therapies Using An shRNA Library Screen.
Sugandha Bhatia, Tony Blick, +9 authors, Erik W Thompson.
Cancers (Basel), 2020 May 06; 12(5). PMID: 32365878    Free PMC article.
Chemogenomic profiling of breast cancer patient-derived xenografts reveals targetable vulnerabilities for difficult-to-treat tumors.
Paul Savage, Alain Pacis, +24 authors, Morag Park.
Commun Biol, 2020 Jun 18; 3(1). PMID: 32546838    Free PMC article.
Exploiting collateral sensitivity controls growth of mixed culture of sensitive and resistant cells and decreases selection for resistant cells in a cell line model.
Vince Kornél Grolmusz, Jinfeng Chen, +5 authors, Andrea H Bild.
Cancer Cell Int, 2020 Jun 23; 20. PMID: 32565737    Free PMC article.
MeCP2 inhibits proliferation and migration of breast cancer via suppression of epithelial-mesenchymal transition.
Wei Jiang, Yan-Ling Liang, +6 authors, Rikang Wang.
J Cell Mol Med, 2020 Jun 09; 24(14). PMID: 32510753    Free PMC article.
Identifying tumor clones in sparse single-cell mutation data.
Matthew A Myers, Simone Zaccaria, Benjamin J Raphael.
Bioinformatics, 2020 Jul 14; 36(Suppl_1). PMID: 32657385    Free PMC article.
Assessing the performance of methods for copy number aberration detection from single-cell DNA sequencing data.
Xian F Mallory, Mohammadamin Edrisi, Nicholas Navin, Luay Nakhleh.
PLoS Comput Biol, 2020 Jul 14; 16(7). PMID: 32658894    Free PMC article.
Circulating Tumor Cells in Metastatic Breast Cancer: From Genome Instability to Metastasis.
Ekaterina Ivanova, Ambber Ward, Adrian P Wiegmans, Derek John Richard.
Front Mol Biosci, 2020 Aug 09; 7. PMID: 32766277    Free PMC article.
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Targeting MYCN-expressing triple-negative breast cancer with BET and MEK inhibitors.
Johanna M Schafer, Brian D Lehmann, +19 authors, Jennifer A Pietenpol.
Sci Transl Med, 2020 Mar 13; 12(534). PMID: 32161105    Free PMC article.
Clinical value and potential mechanisms of COL8A1 upregulation in breast cancer: a comprehensive analysis.
Wei Peng, Jian-Di Li, +9 authors, Gang Chen.
Cancer Cell Int, 2020 Aug 21; 20. PMID: 32818022    Free PMC article.
Single-cell RNA-sequencing reveals distinct patterns of cell state heterogeneity in mouse models of breast cancer.
Syn Kok Yeo, Xiaoting Zhu, +5 authors, Jun-Lin Guan.
Elife, 2020 Aug 26; 9. PMID: 32840210    Free PMC article.
Systems biology approaches to measure and model phenotypic heterogeneity in cancer.
Aaron S Meyer, Laura M Heiser.
Curr Opin Syst Biol, 2020 Aug 31; 17. PMID: 32864511    Free PMC article.
GLUT1 inhibition blocks growth of RB1-positive triple negative breast cancer.
Qin Wu, Wail Ba-Alawi, +26 authors, Cheryl H Arrowsmith.
Nat Commun, 2020 Aug 23; 11(1). PMID: 32826891    Free PMC article.
Targeting poor proteasomal function with radioiodine eliminates CT26 colon cancer stem cells resistant to bortezomib therapy.
Jin Hee Lee, Kyung-Ho Jung, +3 authors, Kyung-Han Lee.
Sci Rep, 2020 Sep 02; 10(1). PMID: 32868872    Free PMC article.
BMI1-Mediated Pemetrexed Resistance in Non-Small Cell Lung Cancer Cells Is Associated with Increased SP1 Activation and Cancer Stemness.
Huan-Ting Shen, Peng-Ju Chien, +4 authors, Wen-Wei Chang.
Cancers (Basel), 2020 Jul 31; 12(8). PMID: 32726929    Free PMC article.
Use of Single-Cell -Omic Technologies to Study the Gastrointestinal Tract and Diseases, From Single Cell Identities to Patient Features.
Mirazul Islam, Bob Chen, +2 authors, Ken S Lau.
Gastroenterology, 2020 May 18; 159(2). PMID: 32417404    Free PMC article.
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Accurate quantification of copy-number aberrations and whole-genome duplications in multi-sample tumor sequencing data.
Simone Zaccaria, Benjamin J Raphael.
Nat Commun, 2020 Sep 04; 11(1). PMID: 32879317    Free PMC article.
Single-Cell Ssequencing in Cancer: Recent Applications to Immunogenomics and Multi-omics Tools.
Michael C Sierant, Jungmin Choi.
Genomics Inform, 2019 Jan 03; 16(4). PMID: 30602078    Free PMC article.
Single-cell analysis of tumors: Creating new value for molecular biomarker discovery of cancer stem cells and tumor-infiltrating immune cells.
Ramin Radpour, Farzad Forouharkhou.
World J Stem Cells, 2019 Jan 12; 10(11). PMID: 30631391    Free PMC article.
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The role of photodynamic therapy on multidrug resistant breast cancer.
Eric Chekwube Aniogo, Blassan Plackal Adimuriyil George, Heidi Abrahamse.
Cancer Cell Int, 2019 Apr 23; 19. PMID: 31007609    Free PMC article.
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Patterns of Mutation Enrichment in Metastatic Triple-Negative Breast Cancer.
César H Saravia, Claudio Flores, +5 authors, Joseph A Pinto.
Clin Med Insights Oncol, 2019 Aug 27; 13. PMID: 31447598    Free PMC article.
Identification of candidate mediators of chemoresponse in breast cancer through therapy-driven selection of somatic variants.
Waleed S Al Amri, Diana E Baxter, +4 authors, Thomas A Hughes.
Breast Cancer Res Treat, 2020 Aug 01; 183(3). PMID: 32734521    Free PMC article.
Identification of Target Genes Related to Sulfasalazine in Triple-Negative Breast Cancer Through Network Pharmacology.
Haochen Yu, Ke Hu, Tao Zhang, Haoyu Ren.
Med Sci Monit, 2020 Sep 15; 26. PMID: 32925871    Free PMC article.
SYTL4 downregulates microtubule stability and confers paclitaxel resistance in triple-negative breast cancer.
Xi-Yu Liu, Wang Jiang, +6 authors, Yi-Zhou Jiang.
Theranostics, 2020 Oct 13; 10(24). PMID: 33042263    Free PMC article.
PhyDOSE: Design of follow-up single-cell sequencing experiments of tumors.
Leah L Weber, Nuraini Aguse, Nicholas Chia, Mohammed El-Kebir.
PLoS Comput Biol, 2020 Oct 02; 16(10). PMID: 33001973    Free PMC article.
MEK inhibition activates STAT signaling to increase breast cancer immunogenicity via MHC-I expression.
Derek A Franklin, Jamaal L James, Margaret L Axelrod, Justin M Balko.
Cancer Drug Resist, 2020 Oct 17; 3. PMID: 33062958    Free PMC article.
Practical classification of triple-negative breast cancer: intratumoral heterogeneity, mechanisms of drug resistance, and novel therapies.
Antonio Marra, Dario Trapani, +2 authors, Giuseppe Curigliano.
NPJ Breast Cancer, 2020 Oct 23; 6. PMID: 33088912    Free PMC article.
Review.
The CXCR4-Dependent LASP1-Ago2 Interaction in Triple-Negative Breast Cancer.
Augustus M C Tilley, Cory M Howard, +4 authors, Dayanidhi Raman.
Cancers (Basel), 2020 Sep 03; 12(9). PMID: 32872485    Free PMC article.
Pathologic evolution-related Gene Analysis based on both single-cell and bulk transcriptomics in Colorectal Cancer.
Jiali Li, Zihang Zeng, +7 authors, Conghua Xie.
J Cancer, 2020 Oct 31; 11(23). PMID: 33123277    Free PMC article.
Clonal Evolution and Timing of Metastatic Colorectal Cancer.
Sarah Siraj, Tariq Masoodi, +13 authors, Khawla S Al-Kuraya.
Cancers (Basel), 2020 Oct 16; 12(10). PMID: 33053768    Free PMC article.
Genomic Instability in Circulating Tumor Cells.
Monique Oliveira Freitas, John Gartner, Aline Rangel-Pozzo, Sabine Mai.
Cancers (Basel), 2020 Oct 22; 12(10). PMID: 33081135    Free PMC article.
Review.
LifeTime and improving European healthcare through cell-based interceptive medicine.
Nikolaus Rajewsky, Geneviève Almouzni, +48 authors, LifeTime Community Working Groups.
Nature, 2020 Sep 08; 587(7834). PMID: 32894860    Free PMC article.
New Insights into Therapy-Induced Progression of Cancer.
Polina V Shnaider, Olga M Ivanova, +6 authors, Victoria O Shender.
Int J Mol Sci, 2020 Oct 30; 21(21). PMID: 33114182    Free PMC article.
Review.
G9a Promotes Breast Cancer Recurrence through Repression of a Pro-inflammatory Program.
Nathaniel W Mabe, Nina Marie G Garcia, +7 authors, James V Alvarez.
Cell Rep, 2020 Nov 05; 33(5). PMID: 33147463    Free PMC article.
Coriolic Acid (13-(S)-Hydroxy-9Z, 11E-octadecadienoic Acid) from Glasswort (Salicornia herbacea L.) Suppresses Breast Cancer Stem Cell through the Regulation of c-Myc.
Yu-Chan Ko, Hack Sun Choi, +3 authors, Dong-Sun Lee.
Molecules, 2020 Oct 30; 25(21). PMID: 33114669    Free PMC article.
Single-Cell Analysis of Different Stages of Oral Cancer Carcinogenesis in a Mouse Model.
Ling-Yu Huang, Yi-Ping Hsieh, +6 authors, Tze-Ta Huang.
Int J Mol Sci, 2020 Nov 05; 21(21). PMID: 33142921    Free PMC article.
I-Impute: a self-consistent method to impute single cell RNA sequencing data.
Xikang Feng, Lingxi Chen, Zishuai Wang, Shuai Cheng Li.
BMC Genomics, 2020 Nov 20; 21(Suppl 10). PMID: 33208097    Free PMC article.
Dietary Energy Modulation and Autophagy: Exploiting Metabolic Vulnerabilities to Starve Cancer.
Alyssa J Cozzo, Michael F Coleman, +3 authors, Stephen D Hursting.
Front Cell Dev Biol, 2020 Nov 24; 8. PMID: 33224954    Free PMC article.
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Breast Cancer Heterogeneity and Response to Novel Therapeutics.
Mariona Baliu-Piqué, Atanasio Pandiella, Alberto Ocana.
Cancers (Basel), 2020 Nov 11; 12(11). PMID: 33167363    Free PMC article.
Review.
Comprehensive Genomic Profile of Heterogeneous Long Follow-Up Triple-Negative Breast Cancer and Its Clinical Characteristics Shows DNA Repair Deficiency Has Better Prognostic.
Ernesto Rojas-Jiménez, Javier César Mejía-Gómez, +18 authors, Felipe Vaca-Paniagua.
Genes (Basel), 2020 Nov 25; 11(11). PMID: 33227964    Free PMC article.
Tumour heterogeneity and metastasis at single-cell resolution.
Devon A Lawson, Kai Kessenbrock, +2 authors, Zena Werb.
Nat Cell Biol, 2018 Nov 30; 20(12). PMID: 30482943    Free PMC article.
Highly Cited. Review.
ddSeeker: a tool for processing Bio-Rad ddSEQ single cell RNA-seq data.
Dario Romagnoli, Giulia Boccalini, +8 authors, Matteo Benelli.
BMC Genomics, 2018 Dec 26; 19(1). PMID: 30583719    Free PMC article.
Overexpression of PARP is an independent prognostic marker for poor survival in Middle Eastern breast cancer and its inhibition can be enhanced with embelin co-treatment.
Abdul Khalid Siraj, Poyil Pratheeshkumar, +5 authors, Khawla S Al-Kuraya.
Oncotarget, 2019 Jan 17; 9(99). PMID: 30647872    Free PMC article.
Co-mutation of TP53 and PIK3CA in residual disease after neoadjuvant chemotherapy is associated with poor survival in breast cancer.
Xinyi Chen, Yonghai Guo, +7 authors, Yuntao Xie.
J Cancer Res Clin Oncol, 2019 Feb 27; 145(5). PMID: 30806788
Dynamin 2, cell trafficking, and the triple-negative paradox.
Sophia B Chernikova, John C Game, J Martin Brown.
Oncotarget, 2019 May 02; 10(24). PMID: 31040924    Free PMC article.
Cellular Metabolic Heterogeneity In Vivo Is Recapitulated in Tumor Organoids.
Joe T Sharick, Justin J Jeffery, +4 authors, Melissa C Skala.
Neoplasia, 2019 May 12; 21(6). PMID: 31078067    Free PMC article.
STAT3 as a potential therapeutic target in triple negative breast cancer: a systematic review.
Jiang-Jiang Qin, Li Yan, Jia Zhang, Wei-Dong Zhang.
J Exp Clin Cancer Res, 2019 May 16; 38(1). PMID: 31088482    Free PMC article.
Highly Cited. Systematic Review.
PI3K inhibition enhances the anti-tumor effect of eribulin in triple negative breast cancer.
Sandeep Rajput, Zhanfang Guo, Shunqiang Li, Cynthia X Ma.
Oncotarget, 2019 Jun 21; 10(38). PMID: 31217901    Free PMC article.
Prognostic impact of PIK3CA protein expression in triple negative breast cancer and its subtypes.
C Elfgen, K Reeve, +5 authors, Z Varga.
J Cancer Res Clin Oncol, 2019 Jul 05; 145(8). PMID: 31270600
The role of clonal communication and heterogeneity in breast cancer.
Ana Martín-Pardillos, Ángeles Valls Chiva, +16 authors, Santiago Ramón Y Cajal.
BMC Cancer, 2019 Jul 07; 19(1). PMID: 31277602    Free PMC article.
When Three Isn't a Crowd: A Digyny Concept for Treatment-Resistant, Near-Triploid Human Cancers.
Kristine Salmina, Bogdan I Gerashchenko, +6 authors, Jekaterina Erenpreisa.
Genes (Basel), 2019 Jul 25; 10(7). PMID: 31331093    Free PMC article.
Review.
Oncogenic TRIM37 Links Chemoresistance and Metastatic Fate in Triple-Negative Breast Cancer.
Piotr Przanowski, Song Lou, +12 authors, Sanchita Bhatnagar.
Cancer Res, 2020 Aug 29; 80(21). PMID: 32855208    Free PMC article.
Systems Biology and Experimental Model Systems of Cancer.
Gizem Damla Yalcin, Nurseda Danisik, Rana Can Baygin, Ahmet Acar.
J Pers Med, 2020 Oct 23; 10(4). PMID: 33086677    Free PMC article.
Review.
Research and application of single-cell sequencing in tumor heterogeneity and drug resistance of circulating tumor cells.
Zhe Dai, Xu-Yu Gu, +3 authors, Yu Fan.
Biomark Res, 2020 Dec 10; 8(1). PMID: 33292625    Free PMC article.
Review.
Evolving insights: how DNA repair pathways impact cancer evolution.
Jiadong Zhou, Xiao Albert Zhou, Ning Zhang, Jiadong Wang.
Cancer Biol Med, 2020 Dec 11; 17(4). PMID: 33299637    Free PMC article.
Review.
Single-cell reconstruction of the adult human heart during heart failure and recovery reveals the cellular landscape underlying cardiac function.
Li Wang, Peng Yu, +8 authors, Shengshou Hu.
Nat Cell Biol, 2020 Jan 10; 22(1). PMID: 31915373
Integrating genetic and non-genetic determinants of cancer evolution by single-cell multi-omics.
Anna S Nam, Ronan Chaligne, Dan A Landau.
Nat Rev Genet, 2020 Aug 19; 22(1). PMID: 32807900
Review.
Digital-WGS: Automated, highly efficient whole-genome sequencing of single cells by digital microfluidics.
Qingyu Ruan, Weidong Ruan, +5 authors, Chaoyong Yang.
Sci Adv, 2020 Dec 11; 6(50). PMID: 33298451    Free PMC article.
miR-613 Suppresses Chemoresistance and Stemness in Triple-Negative Breast Cancer by Targeting FAM83A.
Cuiping Liu, Yizhou Jiang, Baosan Han.
Cancer Manag Res, 2020 Dec 17; 12. PMID: 33324107    Free PMC article.
Genomic and phenotypic heterogeneity in prostate cancer.
Michael C Haffner, Wilbert Zwart, +6 authors, Srinivasan Yegnasubramanian.
Nat Rev Urol, 2020 Dec 18; 18(2). PMID: 33328650    Free PMC article.
Review.
Single-cell analysis of structural variations and complex rearrangements with tri-channel processing.
Ashley D Sanders, Sascha Meiers, +20 authors, Jan O Korbel.
Nat Biotechnol, 2019 Dec 25; 38(3). PMID: 31873213
Single-Cell RNA Sequencing of a Postmenopausal Normal Breast Tissue Identifies Multiple Cell Types That Contribute to Breast Cancer.
Sen Peng, Lora L Hebert, Jennifer M Eschbacher, Suwon Kim.
Cancers (Basel), 2020 Dec 10; 12(12). PMID: 33291647    Free PMC article.
Mechanisms of Resistance to Chemotherapy in Breast Cancer and Possible Targets in Drug Delivery Systems.
Patrícia de Faria Lainetti, Antonio Fernando Leis-Filho, +2 authors, Carlos Eduardo Fonseca-Alves.
Pharmaceutics, 2020 Dec 16; 12(12). PMID: 33316872    Free PMC article.
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A practical guide to cancer subclonal reconstruction from DNA sequencing.
Maxime Tarabichi, Adriana Salcedo, +6 authors, Paul C Boutros.
Nat Methods, 2021 Jan 06; 18(2). PMID: 33398189    Free PMC article.
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Multi-color clonal tracking reveals intra-stage proliferative heterogeneity during mammary tumor progression.
Stefanie Tiede, Ravi Kiran Reddy Kalathur, +8 authors, Gerhard Christofori.
Oncogene, 2020 Oct 14; 40(1). PMID: 33046799
Development of targeted therapy therapeutics to sensitize triple-negative breast cancer chemosensitivity utilizing bacteriophage phi29 derived packaging RNA.
Long Zhang, Chaofeng Mu, +8 authors, Huaqiong Li.
J Nanobiotechnology, 2021 Jan 09; 19(1). PMID: 33413427    Free PMC article.
A `one-two punch' therapy strategy to target chemoresistance in estrogen receptor positive breast cancer.
Feng Chi, Jiayi Liu, +8 authors, Andrea H Bild.
Transl Oncol, 2020 Nov 23; 14(1). PMID: 33221681    Free PMC article.
Adipocytes promote breast tumorigenesis through TAZ-dependent secretion of Resistin.
Yuhao Gao, Xiaosong Chen, +8 authors, Zengqiang Yuan.
Proc Natl Acad Sci U S A, 2020 Dec 16; 117(52). PMID: 33318171    Free PMC article.
Tumour heterogeneity and the evolutionary trade-offs of cancer.
Jean Hausser, Uri Alon.
Nat Rev Cancer, 2020 Feb 26; 20(4). PMID: 32094544
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The Effects of Low HER2/neu Expression on the Clinicopathological Characteristics of Triple-Negative Breast Cancer Patients.
Mehdi Dehghani, Pedram Keshavarz, +4 authors, Maryam Ghanbari.
Asian Pac J Cancer Prev, 2020 Oct 29; 21(10). PMID: 33112563    Free PMC article.
Delineating copy number and clonal substructure in human tumors from single-cell transcriptomes.
Ruli Gao, Shanshan Bai, +14 authors, Nicholas E Navin.
Nat Biotechnol, 2021 Jan 20; 39(5). PMID: 33462507    Free PMC article.
Dormant Tumor Cell Vaccination: A Mathematical Model of Immunological Dormancy in Triple-Negative Breast Cancer.
Reza Mehdizadeh, Seyed Peyman Shariatpanahi, +2 authors, Curzio Rüegg.
Cancers (Basel), 2021 Jan 15; 13(2). PMID: 33440806    Free PMC article.
A High-Dimensional Window into the Micro-Environment of Triple Negative Breast Cancer.
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Review.
Single-cell long noncoding RNA (lncRNA) transcriptome implicates MALAT1 in triple-negative breast cancer (TNBC) resistance to neoadjuvant chemotherapy.
Hibah Shaath, Radhakrishnan Vishnubalaji, +2 authors, Nehad M Alajez.
Cell Death Discov, 2021 Jan 27; 7(1). PMID: 33495450    Free PMC article.
Single-Cell Transcriptomic Heterogeneity in Invasive Ductal and Lobular Breast Cancer Cells.
Fangyuan Chen, Kai Ding, +7 authors, Adrian V Lee.
Cancer Res, 2020 Nov 06; 81(2). PMID: 33148662    Free PMC article.
Erythrocyte membrane-camouflaged carrier-free nanoassembly of FRET photosensitizer pairs with high therapeutic efficiency and high security for programmed cancer synergistic phototherapy.
Xuanbo Zhang, Jianchen Xiong, +12 authors, Jin Sun.
Bioact Mater, 2021 Feb 09; 6(8). PMID: 33553816    Free PMC article.
Characterizing allele- and haplotype-specific copy numbers in single cells with CHISEL.
Simone Zaccaria, Benjamin J Raphael.
Nat Biotechnol, 2020 Sep 04; 39(2). PMID: 32879467
Intratumoral heterogeneity in cancer progression and response to immunotherapy.
Ilio Vitale, Efrat Shema, Sherene Loi, Lorenzo Galluzzi.
Nat Med, 2021 Feb 13; 27(2). PMID: 33574607
Review.
Single-cell RNA-seq dissects the intratumoral heterogeneity of triple-negative breast cancer based on gene regulatory networks.
Shunheng Zhou, Yu-E Huang, +5 authors, Wei Jiang.
Mol Ther Nucleic Acids, 2021 Feb 13; 23. PMID: 33575114    Free PMC article.
Formononetin ameliorates the drug resistance of Taxol resistant triple negative breast cancer by inhibiting autophagy.
Tian Li, Shiyi Zhang, +6 authors, Runwei Tang.
Am J Transl Res, 2021 Feb 18; 13(2). PMID: 33594306    Free PMC article.
Advancing Cancer Research and Medicine with Single-Cell Genomics.
Bora Lim, Yiyun Lin, Nicholas Navin.
Cancer Cell, 2020 Apr 15; 37(4). PMID: 32289270    Free PMC article.
Review.
MEDALT: single-cell copy number lineage tracing enabling gene discovery.
Fang Wang, Qihan Wang, +8 authors, Ken Chen.
Genome Biol, 2021 Feb 25; 22(1). PMID: 33622385    Free PMC article.
Signaling Heterogeneity is Defined by Pathway Architecture and Intercellular Variability in Protein Expression.
Dougall Norris, Pengyi Yang, +8 authors, James G Burchfield.
iScience, 2021 Mar 05; 24(2). PMID: 33659881    Free PMC article.
Molecular subtyping and functional validation of TTK, TPX2, UBE2C, and LRP8 in sensitivity of TNBC to paclitaxel.
Ramesh Elango, Radhakrishnan Vishnubalaji, Hibah Shaath, Nehad M Alajez.
Mol Ther Methods Clin Dev, 2021 Mar 06; 20. PMID: 33665229    Free PMC article.
Recent Advances in Integrative Multi-Omics Research in Breast and Ovarian Cancer.
Christen A Khella, Gaurav A Mehta, Rushabh N Mehta, Michael L Gatza.
J Pers Med, 2021 Mar 07; 11(2). PMID: 33669749    Free PMC article.
Review.
Tumor Heterogeneity: A Great Barrier in the Age of Cancer Immunotherapy.
Nader El-Sayes, Alyssa Vito, Karen Mossman.
Cancers (Basel), 2021 Mar 07; 13(4). PMID: 33671881    Free PMC article.
Review.
Single-cell DNA sequencing reveals complex mechanisms of resistance to quizartinib.
Cheryl A C Peretz, Lisa H F McGary, +7 authors, Catherine C Smith.
Blood Adv, 2021 Mar 06; 5(5). PMID: 33666651    Free PMC article.
Single-cell transcriptional changes associated with drug tolerance and response to combination therapies in cancer.
Alexandre F Aissa, Abul B M M K Islam, +12 authors, Elizaveta V Benevolenskaya.
Nat Commun, 2021 Mar 14; 12(1). PMID: 33712615    Free PMC article.
Methodological Advancements for Investigating Intra-tumoral Heterogeneity in Breast Cancer at the Bench and Bedside.
Mokryun Baek, Jeffrey T Chang, Gloria V Echeverria.
J Mammary Gland Biol Neoplasia, 2020 Dec 11; 25(4). PMID: 33300087    Free PMC article.
Time-Resolved scRNA-Seq Tracks the Adaptation of a Sensitive MCL Cell Line to Ibrutinib Treatment.
Viktoria Fuhr, Ehsan Vafadarnejad, +5 authors, Hilka Rauert-Wunderlich.
Int J Mol Sci, 2021 Mar 07; 22(5). PMID: 33668876    Free PMC article.
Leveraging Single-Cell Approaches in Cancer Precision Medicine.
Aritro Nath, Andrea H Bild.
Trends Cancer, 2021 Feb 11; 7(4). PMID: 33563578    Free PMC article.
Review.
A single-cell atlas of the healthy breast tissues reveals clinically relevant clusters of breast epithelial cells.
Poornima Bhat-Nakshatri, Hongyu Gao, +9 authors, Harikrishna Nakshatri.
Cell Rep Med, 2021 Mar 26; 2(3). PMID: 33763657    Free PMC article.
Clinical epigenetics settings for cancer and cardiovascular diseases: real-life applications of network medicine at the bedside.
Federica Sarno, Giuditta Benincasa, +16 authors, International Network Medicine Consortium.
Clin Epigenetics, 2021 Apr 01; 13(1). PMID: 33785068    Free PMC article.
Review.
Novel Molecular Hallmarks of Group 3 Medulloblastoma by Single-Cell Transcriptomics.
Chaoying Qin, Yimin Pan, +3 authors, Qing Liu.
Front Oncol, 2021 Apr 06; 11. PMID: 33816256    Free PMC article.
Potential Mechanism Underlying the Role of Mitochondria in Breast Cancer Drug Resistance and Its Related Treatment Prospects.
Yuefeng Li, Zhian Li.
Front Oncol, 2021 Apr 06; 11. PMID: 33816265    Free PMC article.
Review.
Leptin and Cancer: Updated Functional Roles in Carcinogenesis, Therapeutic Niches, and Developments.
Tsung-Chieh Lin, Michael Hsiao.
Int J Mol Sci, 2021 Apr 04; 22(6). PMID: 33799880    Free PMC article.
Review.
The Stress-Like Cancer Cell State Is a Consistent Component of Tumorigenesis.
Maayan Baron, Mohita Tagore, +6 authors, Itai Yanai.
Cell Syst, 2020 Sep 11; 11(5). PMID: 32910905    Free PMC article.
Decoding Cancer Biology One Cell at a Time.
L Nicolas Gonzalez Castro, Itay Tirosh, Mario L Suvà.
Cancer Discov, 2021 Apr 04; 11(4). PMID: 33811126    Free PMC article.
Review.
Moss enables high sensitivity single-nucleotide variant calling from multiple bulk DNA tumor samples.
Chuanyi Zhang, Mohammed El-Kebir, Idoia Ochoa.
Nat Commun, 2021 Apr 15; 12(1). PMID: 33850139    Free PMC article.
Unraveling Heterogeneity of Tumor Cells and Microenvironment and Its Clinical Implications for Triple Negative Breast Cancer.
Ke Jiang, Mengting Dong, Chunyang Li, Jiayu Sheng.
Front Oncol, 2021 Apr 16; 11. PMID: 33854958    Free PMC article.
Role of Epigenetic Regulation in Plasticity of Tumor Immune Microenvironment.
Yunkai Yang, Yan Wang.
Front Immunol, 2021 Apr 20; 12. PMID: 33868269    Free PMC article.
Review.
Comprehensive description of the current breast cancer microenvironment advancements via single-cell analysis.
Xueqi Yan, Yinghong Xie, +10 authors, Yongmei Yin.
J Exp Clin Cancer Res, 2021 Apr 29; 40(1). PMID: 33906694    Free PMC article.
Review.
lncRNA GSEC Promotes the Progression of Triple Negative Breast Cancer (TNBC) by Targeting the miR-202-5p/AXL Axis.
Jianhua Zhang, Chuang Du, +3 authors, Jingruo Li.
Onco Targets Ther, 2021 Apr 29; 14. PMID: 33907418    Free PMC article.
Single-cell sequencing techniques from individual to multiomics analyses.
Yukie Kashima, Yoshitaka Sakamoto, +3 authors, Ayako Suzuki.
Exp Mol Med, 2020 Sep 16; 52(9). PMID: 32929221    Free PMC article.
Review.
Functional Roles of SPINK1 in Cancers.
Tsung-Chieh Lin.
Int J Mol Sci, 2021 May 01; 22(8). PMID: 33916984    Free PMC article.
Review.
From Oncogenic Signaling Pathways to Single-Cell Sequencing of Immune Cells: Changing the Landscape of Cancer Immunotherapy.
Afshin Derakhshani, Zeinab Rostami, +12 authors, Behzad Baradaran.
Molecules, 2021 May 01; 26(8). PMID: 33920054    Free PMC article.
Review.
Optimizing individualized treatment strategy based on breast cancer organoid model.
Bo Pan, Xuelu Li, +4 authors, Zuowei Zhao.
Clin Transl Med, 2021 May 02; 11(4). PMID: 33931968    Free PMC article.
CXCL1 Clone Evolution Induced by the HDAC Inhibitor Belinostat Might Be a Favorable Prognostic Indicator in Triple-Negative Breast Cancer.
Xin-le Han, Jun Du, +8 authors, Zheng-Yu Fang.
Biomed Res Int, 2021 May 08; 2021. PMID: 33959656    Free PMC article.
Image-Based Live Cell Sorting.
Cody A LaBelle, Angelo Massaro, +2 authors, Nancy L Allbritton.
Trends Biotechnol, 2020 Nov 17; 39(6). PMID: 33190968    Free PMC article.
Review.
RIPK1 is a negative mediator in Aquaporin 1-driven triple-negative breast carcinoma progression and metastasis.
Zhuming Yin, Wenlin Chen, +5 authors, Huiwen Ren.
NPJ Breast Cancer, 2021 May 14; 7(1). PMID: 33980862    Free PMC article.
Single cell RNA sequencing for breast cancer: present and future.
Lili Ren, Junyi Li, +8 authors, Jing Tang.
Cell Death Discov, 2021 May 16; 7(1). PMID: 33990550    Free PMC article.
Review.
Integrative single-cell analysis of allele-specific copy number alterations and chromatin accessibility in cancer.
Chi-Yun Wu, Billy T Lau, +4 authors, Nancy R Zhang.
Nat Biotechnol, 2021 May 22;. PMID: 34017141
Modeling clonal structure over narrow time frames via circulating tumor DNA in metastatic breast cancer.
Zachary T Weber, Katharine A Collier, +16 authors, Daniel G Stover.
Genome Med, 2021 May 22; 13(1). PMID: 34016182    Free PMC article.
Dissecting intratumour heterogeneity of nodal B-cell lymphomas at the transcriptional, genetic and drug-response levels.
Tobias Roider, Julian Seufert, +23 authors, Sascha Dietrich.
Nat Cell Biol, 2020 Jun 17; 22(7). PMID: 32541878
Single-cell RNA sequencing in cancer: Applications, advances, and emerging challenges.
Guangshun Sun, Zhouxiao Li, +9 authors, Yangbai Sun.
Mol Ther Oncolytics, 2021 May 25; 21. PMID: 34027052    Free PMC article.
Review.
The many faces of cancer evolution.
Giovanni Ciriello, Luca Magnani.
iScience, 2021 May 25; 24(5). PMID: 34027317    Free PMC article.
Review.
Phenotypic Heterogeneity of Triple-Negative Breast Cancer Mediated by Epithelial-Mesenchymal Plasticity.
Barbora Kvokačková, Ján Remšík, Mohit Kumar Jolly, Karel Souček.
Cancers (Basel), 2021 Jun 03; 13(9). PMID: 34063254    Free PMC article.
Review.