Cited by 1,973Cancer Cells and MetastasisBreast Cancer Treatment Studies3D Printing in Biomedical Research

The DOI matches its Crossref record; 75 of the 79 references it cites were found in a registry or an index.

A Living Biobank of Breast Cancer Organoids Captures Disease Heterogeneity

Open access

Sachs, Norman, de Ligt, Joep, Kopper, Oded, Gogola, Ewa, Bounova, Gergana, Weeber, Fleur, Balgobind, Anjali Vanita, Wind, Karin, Gracanin, Ana, Begthel, Harry, Korving, Jeroen, van Boxtel, Ruben, Duarte, Alexandra Alves, Lelieveld, Daphne, van Hoeck, Arne, Ernst, Robert Frans, Blokzijl, Francis, Nijman, Isaac Johannes, Hoogstraat, Marlous, van de Ven, Marieke, Egan, David Anthony, Zinzalla, Vittoria, Moll, Jurgen, Boj, Sylvia Fernandez, Voest, Emile Eugene, Wessels, Lodewyk, van Diest, Paul Joannes, Rottenberg, Sven, Vries, Robert Gerhardus Jacob, Cuppen, Edwin, Clevers, Hans·2018·Cell

DOI 10.1016/j.cell.2017.11.010

Open this paper in CoChat — free account Open PDF

Abstract

Breast cancer (BC) comprises multiple distinct subtypes that differ genetically, pathologically, and clinically. Here, we describe a robust protocol for long-term culturing of human mammary epithelial organoids. Using this protocol, >100 primary and metastatic BC organoid lines were generated, broadly recapitulating the diversity of the disease. BC organoid morphologies typically matched the histopathology, hormone receptor status, and HER2 status of the original tumor. DNA copy number variations as well as sequence changes were consistent within tumor-organoid pairs and largely retained even after extended passaging. BC organoids furthermore populated all major gene-expression-based classification groups and allowed in vitro drug screens that were consistent with in vivo xeno-transplantations and patient response. This study describes a representative collection of well-characterized BC organoids available for cancer research and drug development, as well as a strategy to assess in vitro drug response in a personalized fashion.

Integrity signals

Registry

Crossref · 10.1016/j.cell.2017.11.010

Cites

75 of 75 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

The text we found for this paper looks like another document, so its claims and self-check weren’t run. The registry and citation checks still apply.

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The text we found for this paper looks like another document, so the self-check wasn’t run.

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010) · Genome Research · doi:10.1101/gr.107524.110 · Cited by 27,895
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464
Comprehensive molecular portraits of human breast tumours
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11412 · Cited by 12,129
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w 1118 ; iso-2; iso-3
Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (2012) · Fly · doi:10.4161/fly.19695 · Cited by 11,816
Signatures of mutational processes in human cancer
Initiative, A. P. C. G., Alexandrov, L. B., ICGC Breast Cancer Consortium, ICGC MMML-Seq Consortium, PedBrain, I., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., Behjati, S., Biankin, A. V., et al. (2013) · Nature · doi:10.1038/nature12477 · Cited by 9,660
Adjusting batch effects in microarray expression data using empirical Bayes methods
Johnson, W. E., Li, C., & Rabinovic, A. (2007) · Biostatistics · doi:10.1093/biostatistics/kxj037 · Cited by 8,658
dbSNP: the NCBI database of genetic variation
Sherry, S. T. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.1.308 · Cited by 7,502

Flagged first, then by citations

Show all 79 references

4 of the 79 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

Blokzijl, 2016, MutationalPatterns: an integrative R package for studying patterns in base substitution catalogues, bioRxiv

Sorted by citations

Items 901–1,000 of 1,002

Kidney organoids as a promising tool in nephrology
Wu, M., Hu, T., Zhu, P., Nasser, M. I., Shen, J., Sun, F., He, Q., & Zhao, M. (2021) · Genes & Diseases · doi:10.1016/j.gendis.2021.01.003 · Cited by 16
A Perspective on a Urine-Derived Kidney Tubuloid Biobank from Patients with Hereditary Tubulopathies
Schutgens, F., Rookmaaker, M. B., & Verhaar, M. C. (2021) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2020.0366 · Cited by 14
Progress and perspective of organoid technology in cancer-related translational medicine
Lin, Y., Jiang, L., He, Q., Yuan, M., & Cao, J. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.112869 · Cited by 18
Patient-derived organoids as a model for tumor research
Wang, J., Feng, X., Li, Z., Chen, Y., & Huang, W. (2022) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2022.03.004 · Cited by 15
Tumor Organoids as a Research Tool: How to Exploit Them
Booij, T. H., Cattaneo, C. M., & Hirt, C. (2022) · Cells · doi:10.3390/cells11213440 · Cited by 17
Inonotsutriol E from Inonotus obliquus exhibits promising anti breast cancer activity via regulating the JAK2/STAT3 signaling pathway
Shan, P., Wang, C., Chen, H., Yu, J., & Zhang, H. (2023) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2023.106741 · Cited by 19
YAP/TAZ-mediated regulation of laminin 332 is enabled by β4 integrin repression of ZEB1 to promote ferroptosis resistance
Goel, H. L., Karner, E. R., Kumar, A., et al. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107202 · Cited by 15
Advanced Hydrogels in Breast Cancer Therapy
Gao, X., Caruso, B. R., & Li, W. (2024) · Gels · doi:10.3390/gels10070479 · Cited by 17
The potential and challenges of patient-derived organoids in guiding the multimodality treatment of upper gastrointestinal malignancies
Busslinger, G. A., Lissendorp, F., Franken, I. A., van Hillegersberg, R., Ruurda, J. P. H., Clevers, H. C., & de Maat, M. F. G. (2020) · Open Biology · doi:10.1098/rsob.190274 · Cited by 15
Self-citation
RNA sequencing of long-term label-retaining colon cancer stem cells identifies novel regulators of quiescence
Regan, J. L., Schumacher, D., Staudte, S., Steffen, A., Lesche, R., Toedling, J., Jourdan, T., Haybaeck, J., Mumberg, D., Henderson, D. A., et al. (2021) · iScience · doi:10.1016/j.isci.2021.102618 · Cited by 17
A gentle introduction to understanding preclinical data for cancer pharmaco-omic modeling
Piyawajanusorn, C., Nguyen, L. C., Ghislat, G., & Ballester, P. J. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab312 · Cited by 18
NSG-Pro mouse model for uncovering resistance mechanisms and unique vulnerabilities in human luminal breast cancers
Sun, Y., Yang, N., Utama, F. E., Udhane, S. S., Zhang, J., Peck, A. R., Yanac, A. F., Duffey, K. E., Langenheim, J. F., Udhane, V., et al. (2021) · Science Advances · doi:10.1126/sciadv.abc8145 · Cited by 15
An Aging-Related Gene Signature-Based Model for Risk Stratification and Prognosis Prediction in Breast Cancer
Yuan, J., Duan, F., Zhai, W., Song, C., Wang, L., Xia, W., Hua, X., Yuan, Z., Bi, X., & Huang, J. (2021) · International Journal of Women s Health · doi:10.2147/ijwh.s334756 · Cited by 14
Focus on organoids: cooperation and interconnection with extracellular vesicles – Is this the future of in vitro modeling?
Jurj, A. M., Paşca, S., Braicu, C., Rusu, I., Korban, S. S., & Berindan‐Neagoe, I. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.12.002 · Cited by 15
Use of conditional reprogramming cell, patient derived xenograft and organoid for drug screening for individualized prostate cancer therapy: Current and future perspectives (Review)
Cao, J., Chan, W. H., & Chow, M. (2022) · International Journal of Oncology · doi:10.3892/ijo.2022.5342 · Cited by 15
Establishing Human Lung Organoids and Proximal Differentiation to Generate Mature Airway Organoids
Li, C., Chiu, M. C., Yu, Y., Liu, X., Xiao, D., Huang, J., Wan, Z., & Zhou, J. (2022) · Journal of Visualized Experiments · doi:10.3791/63684 · Cited by 19
Advances of Patient-Derived Organoids in Personalized Radiotherapy
Wang, Y., Li, Y., Sheng, Z., Deng, W., Yuan, H., Wang, S., & Liu, Y. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.888416 · Cited by 19
Brain Tumor Biobank Development for Precision Medicine: Role of the Neurosurgeon
Darrigues, E., Elberson, B. W., Loose, A. D., Lee, M. P., Green, E., Benton, A. M., Sink, L. G., Scott, H. W., Gökden, M., Day, J. D., et al. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.662260 · Cited by 15
Therapeutic induction of ferroptosis in tumors using PD-L1 targeting antibody nanogel conjugates
Wang, M., Prachyathipsakul, T., Silva, C. A., Xiong, C., Goel, S., Goel, H. L., Karner, E. R., Mukhopadhyay, D., Gupta, P., Majee, A., et al. (2024) · Cell chemical biology · doi:10.1016/j.chembiol.2024.10.014 · Cited by 14
Generation of prostate cancer assembloids modeling the patient-specific tumor microenvironment
Lee, J.-H., Kim, Y., Lee, C. M., Jeon, S. S., Seo, H. K., Lee, J. W., Choi, J., Kang, M., Kim, E., & Shin, K. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011652 · Cited by 14
Innovative organ-on-a-chip platforms for exploring tumorigenesis and therapy in head and neck cancer
Lin, C., Zhang, Z., Yang, F. L., Gu, S., Zuo, J., Wu, Y. M., Zhang, J., Zhou, T., Zhang, Y., Chen, Z., et al. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06824-5 · Cited by 14
Intersection of ferroptosis and nanomaterials brings benefits to breast cancer
Gao, J., Ma, N., Ni, S., & Han, X. F. (2025) · Cell Biology and Toxicology · doi:10.1007/s10565-025-10067-x · Cited by 17
Organoids as predictive platforms: advancing disease modeling, therapeutic innovation, and drug delivery systems
Huang, T. H., Huang, W. T., & Bian, Q. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.114222 · Cited by 14
Understanding of tumourigenesis in canine mammary tumours based on cancer stem cell research
Michishita, M. (2020) · The Veterinary Journal · doi:10.1016/j.tvjl.2020.105560 · Cited by 14
Breast cancer prevention by short-term inhibition of TGFβ signaling
Alečković, M., Cristea, S., del Alcazar, C. R. G., Yan, P., Ding, L., Krop, E. D., Harper, N. W., Rojas-Jiménez, E. A., Lu, D., Gulvady, A. C., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-35043-5 · Cited by 14
Vaginal Bacteria Elicit Acute Inflammatory Response in Fallopian Tube Organoids
Yu, B., Nguyen, E. B., McCartney, S., Strenk, S., Valint, D., Liu, C., Haggerty, C., & Fredricks, D. N. (2023) · Reproductive Sciences · doi:10.1007/s43032-023-01350-5 · Cited by 15
Three-Dimensional Tumor Models to Study Cancer Stemness-Mediated Drug Resistance
Lamichhane, A., & Tavana, H. (2024) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-024-00798-y · Cited by 16
Clinical efficacy of tumor organoid‐guided cancer therapy for locally advanced unresectable or metastatic breast cancer
Lin, Y., Gao, H., Li, H., Hu, Q., Du, B., Li, S., Xu, F., Cheng, M., Zou, J., Zheng, X., et al. (2024) · International Journal of Cancer · doi:10.1002/ijc.34945 · Cited by 15
The combination of breast cancer PDO and mini‐PDX platform for drug screening and individualized treatment
Cui, Y., Ran, R., Da, Y., Zhang, H., Jiang, M., Qi, X., Zhang, W., Niu, L., Zhou, C., Zhou, C., et al. (2024) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.18374 · Cited by 14
Cancer research revolutionized: Unveiling the power of organoids and their therapeutic potential in oncology
Zhang, Y., Liu, M., Xie, N., Wang, Z., Yu, C., Li, J., & Zhou, X. (2024) · hLife · doi:10.1016/j.hlife.2024.05.002 · Cited by 17
Centralized intestinal organoid generation is a feasible and safe approach for personalized medicine as demonstrated in the HIT-CF Europe Organoid Study
Bierlaagh, M. C., van Mourik, P., Vonk, A. M., Pott, J., Muilwijk, D., Berkers, G., Aalbers, B. L., Vleggaar, F. P., Heida-Michel, S., Boj, S. F., et al. (2024) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2024.04.016 · Cited by 14
Self-citation
Progress and application of lung-on-a-chip for lung cancer
Li, L., Bo, W., Wang, G., Juan, X., Xue, H., & Zhang, H. (2024) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2024.1378299 · Cited by 14
In vivo organoid growth monitoring by stimulated Raman histology
Sarri, B., Chevrier, V., Poizat, F., Heuke, S., Franchi, F., de Franqueville, L., Traversari, E., Ratone, J., Caillol, F., Dahel, Y., et al. (2024) · npj Imaging · doi:10.1038/s44303-024-00019-1 · Cited by 15
Identification of functional biomarkers for personalized nanomedicine in advanced breast cancer in vitro models
Boix-Montesinos, P., Carrascosa-Marco, P., Armiñán, A., et al. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113584 · Cited by 14
Conditional cell reprogramming for modeling host‐virus interactions and human viral diseases
Liu, X., & Mondal, A. M. (2020) · Journal of Medical Virology · doi:10.1002/jmv.26093 · Cited by 13
Applications of Omics Technologies for Three-Dimensional In Vitro Disease Models
Pieters, V. M., Co, I. L., Wu, N. C., & McGuigan, A. P. (2021) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2020.0300 · Cited by 14
Arctigenin inhibits human breast cancer cell proliferation, migratory and invasive abilities and epithelial to mesenchymal transition by targeting 4EBP1
Luo, W., Wang, F., Luo, H., et al. (2021) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2021.9979 · Cited by 14
Instructive Hydrogels for Primary Tumor Cell Culture: Current Status and Outlook
Jia, Y., Wei, Z., Zhang, S., Yang, B., & Li, Y. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202102479 · Cited by 13
Application of tumoroids derived from advanced colorectal cancer patients to predict individual response to chemotherapy
Yao, L., Zao, X.-L., Pan, X.-F., Zhang, H.-G., Wang, F.-J., & Qiao, P.-F. (2022) · Journal of Chemotherapy · doi:10.1080/1120009x.2022.2045827 · Cited by 13
Advances in the use of 3D colorectal cancer models for novel drug discovery
Baião, A., Dias, S., Soares, A. F., Pereira, C. L., Oliveíra, C., & Sarmento, B. F. C. C. (2022) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2022.2056162 · Cited by 13
Kinome Reprogramming Is a Targetable Vulnerability in ESR1 Fusion-Driven Breast Cancer
Gou, X., Kim, B.-J., Anurag, M., Lei, J. T., Young, M. N., Holt, M. V., Fandino, D. M., Vollert, C. T., Singh, P., Alzubi, M. A., et al. (2023) · Cancer Research · doi:10.1158/0008-5472.can-22-3484 · Cited by 14
Remodelling and Improvements in Organoid Technology to Study Liver Carcinogenesis in a Dish
Tharehalli, U., Svinarenko, M., & Lechel, A. (2019) · Stem Cells International · doi:10.1155/2019/3831213 · Cited by 15
QPI Allows in vitro Drug Screening of Triple Negative Breast Cancer PDX Tumors and Fine Needle Biopsies
Murray, G. F., Turner, T. H., Guest, D. C., et al. (2019) · Frontiers in Physics · doi:10.3389/fphy.2019.00158 · Cited by 14
Modeling chemical effects on breast cancer: the importance of the microenvironment in vitro
Morgan, M. M., Schuler, L. A., Ciciliano, J. C., Johnson, B. P., Alarid, E. T., & Beebe, D. J. (2020) · Integrative Biology · doi:10.1093/intbio/zyaa002 · Cited by 14
Single and double modified salinomycin analogs target stem-like cells in 2D and 3D breast cancer models
Urbaniak, A. J., Reed, M. R., Fil, D., Moorjani, A., Heflin, S., Antoszczak, M., Sulik, M., Huczyński, A., Kupsik, M., Eoff, R. L., et al. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111815 · Cited by 14
Modelling adult stem cells and their niche in health and disease with epithelial organoids
Szabó, L., Seubert, A. C., & Kretzschmar, K. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.09.006 · Cited by 14
A hollow fiber membrane-based liver organoid-on-a-chip model for examining drug metabolism and transport
Myszczyszyn, A., Muench, A., Lehmann, V., Sinnige, T., van Steenbeek, F. G., Bouwmeester, M., Samsom, R.-A., Keuper-Navis, M., van der Made, T. K., Kogan, D., et al. (2025) · Biofabrication · doi:10.1088/1758-5090/adc3ce · Cited by 14
Modeling epithelial-mesenchymal transition in patient-derived breast cancer organoids
Bar-Hai, N., Ben-Yishay, R., Arbili-Yarhi, S., Herman, N., Noy, V., Menes, T. S., Mansour, A., Awwad, F., Balint‐Lahat, N., Goldinger, G., et al. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1470379 · Cited by 13
Memory-promoting function of miR-379-5p attenuates CD8+ T cell exhaustion by targeting immune checkpoints
Lin, Y.-Z., Liu, C.-H., Wu, W., Liao, T.-Y., Lee, C.-C., Li, H., Chung, F.-C., Shen, Y.-C., Zhuo, G., Liu, L., et al. (2025) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2024-010363 · Cited by 13
SNX10 deficiency impairs sensitivity to anti-HER2 antibody–drug conjugates via altering HER2 trafficking in HER2-positive breast cancer
Chen, Y.-F., Zhang, Q., Zhang, Z., Zhou, Y.-J., Liu, C., Shao, Z.-M., & Yu, K. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2417586122 · Cited by 16
A subcellular cookie cutter for spatial genomics in human tissue
Bury, A. G., Pyle, A., Marcuccio, F., et al. (2022) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-022-03944-5 · Cited by 13
PHF6 recruits BPTF to promote HIF-dependent pathway and progression in YAP-high breast cancer
Gao, S., Zhang, W., Ma, J., et al. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04031-8 · Cited by 13
Patient-derived xenografts or organoids in the discovery of traditional and self-assembled drug for tumor immunotherapy
Zhang, W., & Zheng, X. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1122322 · Cited by 15
Organoids as an Enabler of Precision Immuno-Oncology
Zhao, J., Fong, A. S. W., Seow, S. V., & Toh, H. C. (2023) · Cells · doi:10.3390/cells12081165 · Cited by 13
Gynecologic and Breast Cancers: What's New in Chemoresistance and Chemosensitivity Tests?
Marcolin, J. C., Lichtenfels, M., Silva, C. A., & de Farias, C. B. (2023) · Current Problems in Cancer · doi:10.1016/j.currproblcancer.2023.100996 · Cited by 13
Organoid models of the pituitary gland in health and disease
Laporte, E., & Vankelecom, H. E. J. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1233714 · Cited by 15
Exploiting a living biobank to delineate mechanisms underlying disease-specific chromosome instability
Nelson, L., Barnes, B. M., Tighe, A., Littler, S., Coulson‐Gilmer, C., Golder, A., Desai, S. N., Morgan, R. D., McGrail, J. C., & Taylor, S. S. (2023) · Chromosome Research · doi:10.1007/s10577-023-09731-x · Cited by 13
Human Breast Organoid Models for Lactation Research
Lee, J., Liu, Y., Ray, E. E., Giuliano, A., & Cui, X.-J. (2023) · Reproduction and Breeding · doi:10.1016/j.repbre.2023.08.003 · Cited by 13
Application of organoids in precision immunotherapy of lung cancer (Review)
Tian, H., Ren, J., Mou, R., & Jia, Y. (2023) · Oncology Letters · doi:10.3892/ol.2023.14071 · Cited by 14
Integrated transcriptomics, proteomics, and functional analysis to characterize the tissue‐specific small extracellular vesicle network of breast cancer
Shen, L., Huang, H., Wei, Z., Chen, W., Li, J., Yao, Y., Zhou, J., Liu, J., Sun, S., Xia, W., et al. (2023) · MedComm · doi:10.1002/mco2.433 · Cited by 12
Establishment of a novel overlay culture method that enables immune response assessment using gastric cancer organoids
Ota, H., Tanabe, K., Saeki, Y., Takemoto, Y., Chikuie, E., Tanaka, Y., Sakamoto, N., & Ohdan, H. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e23520 · Cited by 13
Establishing mesothelioma patient-derived organoid models from malignant pleural effusions
Hocking, A. J., Mortimer, L. A., Farrall, A. L., Russell, P. A., & Klebe, S. (2024) · Lung Cancer · doi:10.1016/j.lungcan.2024.107542 · Cited by 13
U-Shape Pillar Strip for 3D Cell-Lumped Organoid Model (3D-COM) Mimicking Lung Cancer Hypoxia Conditions in High-Throughput Screening (HTS)
Lee, S., Lee, E., Lim, J. U., et al. (2024) · Analytical Chemistry · doi:10.1021/acs.analchem.4c00890 · Cited by 13
Breast cancer patient-derived organoids for the investigation of patient-specific tumour evolution
Mazzucchelli, S., Signati, L., Messa, L., Franceschini, A., Bonizzi, A., Castagnoli, L., Gasparini, P., Consolandi, C., Mangano, E., Pelucchi, P., et al. (2024) · Cancer Cell International · doi:10.1186/s12935-024-03375-5 · Cited by 14
Interpretation of the past, present, and future of organoid technology: an updated bibliometric analysis from 2009 to 2024
Qu, B., Mu, Q., Bi, H., Chen, Y., Wang, Q., Ma, X., & Lu, L. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1433111 · Cited by 13
Precision preclinical modeling to advance cancer treatment
Gutmann, D. H., Boehm, J. S., Karlsson, E. K., Padron, E., Seshadri, M., WALLIS, D. E., & Snyder, J. C. (2024) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djae249 · Cited by 14
Tumor organoids in cancer medicine: from model systems to natural compound screening
Cong, R., Lu, C., Li, X., Xu, Z., Wang, Y., & Sun, S. (2025) · Pharmaceutical Biology · doi:10.1080/13880209.2025.2458149 · Cited by 16
Single-cell organogenesis captures complex breast tissue formation in three dimensions
Rauner, G., Traugh, N. C., Trepicchio, C. J., Parrish, M. E., Mushayandebvu, K., & Kuperwasser, C. (2025) · Development · doi:10.1242/dev.204813 · Cited by 13
Modeling Hematological Diseases and Cancer With Patient-Specific Induced Pluripotent Stem Cells
Kim, H., & Schaniel, C. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02243 · Cited by 14
The Mini‐Organo: A rapid high‐throughput 3D coculture organotypic assay for oncology screening and drug development
Chitty, J. L., Skhinas, J. N., Filipe, E. C., Wang, S., Cupello, C. R., Grant, R. D., Yam, M., Papanicolaou, M., Major, G. S., Zaratzian, A., et al. (2019) · Cancer Reports · doi:10.1002/cnr2.1209 · Cited by 13
Personalized Assessment of Normal Tissue Radiosensitivity via Transcriptome Response to Photon, Proton and Carbon Irradiation in Patient-Derived Human Intestinal Organoids
Nowrouzi, A., Sertorio, M. G., Akbarpour, M., Knoll, M., Krunic, D., Kuhar, M., Schwager, C., Brons, S., Debus, J., Wells, S. I., et al. (2020) · Cancers · doi:10.3390/cancers12020469 · Cited by 14
Future Match Making: When Pediatric Oncology Meets Organoid Technology
Barbet, V., & Broutier, L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.674219 · Cited by 19
Recapitulating the Cancer Microenvironment Using Bioprinting Technology for Precision Medicine
Kim, J., Jang, J., & Cho, D. (2021) · Micromachines · doi:10.3390/mi12091122 · Cited by 13
Use of Patient-Derived Organoids as a Treatment Selection Model for Colorectal Cancer: A Narrative Review
Furbo, S., Urbano, P. C. M., Raskov, H., Troelsen, J. T., Fiehn, A. K., & Gögenür, I. (2022) · Cancers · doi:10.3390/cancers14041069 · Cited by 13
Transcriptional Factor Repertoire of Breast Cancer in 3D Cell Culture Models
Özkan, H., Öztürk, D. G., & Korkmaz, G. (2022) · Cancers · doi:10.3390/cancers14041023 · Cited by 14
Stem Cell Models for Cancer Therapy
TELANG, N. T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137055 · Cited by 13
Microfluidic Biosensor-Based Devices for Rapid Diagnosis and Effective Anti-cancer Therapeutic Monitoring for Breast Cancer Metastasis
Sudhakaran, S. V., & Rath, S. N. (2022) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-04039-9_13 · Cited by 13
Live Cell Mass Accumulation Measurement Non-Invasively Predicts Carboplatin Sensitivity in Triple-Negative Breast Cancer Patient-Derived Xenografts
Murray, G. F., Turner, T. H., Leslie, K. A., Alzubi, M. A., Guest, D. C., Sohal, S. S., Teitell, M. A., Harrell, J. C., & Reed, J. C. (2018) · ACS Omega · doi:10.1021/acsomega.8b02224 · Cited by 13
Reflection of neuroblastoma intratumor heterogeneity in the new OHC‐NB1 disease model
Thole-Kliesch, T. M., Toedling, J., Sprüssel, A., Pfeil, S., Savelyeva, L., Capper, D., Messerschmidt, C., Beule, D., Groeneveld‐Krentz, S., Eckert, C., et al. (2019) · International Journal of Cancer · doi:10.1002/ijc.32572 · Cited by 13
Liver Buds and Liver Organoids: New Tools for Liver Development, Disease and Medical Application
Zeng, F., Zhang, Y., Han, X., Weng, J., & Gao, Y. (2019) · Stem Cell Reviews and Reports · doi:10.1007/s12015-019-09909-z · Cited by 13
Organoids as Complex In Vitro Models for Studying Radiation-Induced Cell Recruitment
Hacker, B. C., & Rafat, M. (2020) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-020-00625-0 · Cited by 15
Optimal, Large-Scale Propagation of Mouse Mammary Tumor Organoids
Wrenn, E. D., Moore, B. M., Greenwood, E., McBirney, M., & Cheung, K. J. (2020) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-020-09464-1 · Cited by 14
Configurational entropy is an intrinsic driver of tissue structural heterogeneityPreprint
Srivastava, V., Hu, J. L., Garbe, J. C., Veytsman, B. A., Shalabi, S., Yllanes, D., Thomson, M. W., LaBarge, M. A., Huber, G., & Gartner, Z. J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.01.546933 · Cited by 14
Organoid Cultures for the Study of Mammary Biology and Breast Cancer: The Promise and ChallengesPreprint
Muthuswamy, S. K., & Brugge, J. S. (2023) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041661 · Cited by 13
Human milk: insights on cell composition, organoids and emerging applications
Majood, M., & Rao, R. (2025) · Pediatric Research · doi:10.1038/s41390-025-04458-3 · Cited by 12
Organoid research: new concepts and new technologies
Zhang, J., Wu, Y., Shen, T., Mao, Y., Dou, H., Lin, Y., Geng, Z., Li, Z., & Su, J. (2026) · Burns & Trauma · doi:10.1093/burnst/tkag015 · Cited by 20
Organs-on-Chips in Drug Development: Engineering Foundations, Artificial Intelligence, and Clinical Translation
Roy, N., & Cucullo, L. (2026) · Biosensors · doi:10.3390/bios16030155 · Cited by 16
The CellRaft AIRⓇ system: A novel system enabling organoid imaging, identification, and isolation
Stern, A., Thompson, B., Williams, K., McClellan, R., Gebhart, S., & Hartman, J. (2022) · SLAS DISCOVERY · doi:10.1016/j.slasd.2021.11.003 · Cited by 11
Translational and Clinical Relevance of PDX‐Derived Organoid Models in Oncology Drug Discovery and Development
Kumari, R., Xu, X., & Li, H. (2022) · Current Protocols · doi:10.1002/cpz1.431 · Cited by 13
Establishing Bipotential Human Lung Organoid Culture System and Differentiation to Generate Mature Alveolar and Airway Organoids
Chiu, M. C., Li, C., Yu, Y., Liu, X., Huang, J., Wan, Z., Yuen, K.-Y., & Zhou, J. (2023) · BIO-PROTOCOL · doi:10.21769/bioprotoc.4657 · Cited by 13
Three-dimensional bioprinting of in vitro tumor organoid and organ-on-a-chip models
Anderson, S. R., Stagner, E., Sivakumar, H., & Skardal, A. (2023) · MRS Bulletin · doi:10.1557/s43577-023-00559-8 · Cited by 12
Spatial -omics technologies: the new enterprise in 3D breast cancer models
Pierantoni, L., Reis, R. L., Silva‐Correia, J., Oliveira, J. M., & Heavey, S. (2023) · Trends in biotechnology · doi:10.1016/j.tibtech.2023.07.003 · Cited by 12
Can Organoid Model Reveal a Key Role of Extracellular Vesicles in Tumors? A Comprehensive Review of the Literature
Zhang, Y., Lu, A., Zhuang, Z., Zhang, S., Liu, S., Chen, H., Yang, X., & Wang, Z. (2023) · International Journal of Nanomedicine · doi:10.2147/ijn.s424737 · Cited by 14
Single-Cell Transcription Mapping of Murine and Human Mammary Organoids Responses to Female Hormones
Ortiz, J. R., Lewis, S. M., Ciccone, M. F., Chatterjee, D., Henry, S., Siepel, A. C., & dos Santos, C. O. (2024) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-023-09553-x · Cited by 13
State of the Art Modelling of the Breast Cancer Metastatic Microenvironment: Where Are We?
Nuckhir, M., Withey, D., Cabral, S. C. M., Harrison, H., & Clarke, R. B. (2024) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-024-09567-z · Cited by 14
Gastrointestinal Cancer Patient Derived Organoids at the Frontier of Personalized Medicine and Drug Screening
Yang, Z., Yu, J. Q., & Wong, C. C. (2024) · Cells · doi:10.3390/cells13161312 · Cited by 12
Essential gene screening identifies the bromodomain-containing protein BRPF1 as a new actionable target for endocrine therapy-resistant breast cancers
Salvati, A., Giurato, G., Lamberti, J., Terenzi, I., Crescenzo, L., Melone, V., Palo, L., Giordano, A., Sabbatino, F., Roscigno, G., et al. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02071-2 · Cited by 12
Single-cell chemoproteomics identifies metastatic activity signatures in breast cancer
Pillai, K. S., Laxton, O. C., Li, G., Lin, J., Karginova, O. A., Nanda, R., Olopade, O. I., Tay, S., & Moellering, R. E. (2024) · Science Advances · doi:10.1126/sciadv.adp2622 · Cited by 12
Metabolic profiling of patient-derived organoids reveals nucleotide synthesis as a metabolic vulnerability in malignant rhabdoid tumors
Kes, M. M. G., Morales-Rodriguez, F., Zaal, E. A., de Souza, T. M., Proost, N., van de Ven, M., van den Heuvel‐Eibrink, M. M., Jansen, J. W. A., Berkers, C. R., & Drost, J. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101878 · Cited by 13
RNF31 induces paclitaxel resistance by sustaining ALYREF cytoplasmic–nuclear shuttling in human triple‐negative breast cancer
Huang, S., Shi, D., Dai, S., Jiang, X., Wang, R., Yang, M., Chen, B., Chen, X., Kong, L., He, L., et al. (2025) · Clinical and Translational Medicine · doi:10.1002/ctm2.70203 · Cited by 12

Authors: Sachs, N., de Ligt, J., Kopper, O., Gogola, E., Bounova, G., Weeber, F., Balgobind, A. V., Wind, K., Gracanin, A., Begthel, H., Korving, J., van Boxtel, R., Duarte, A. A., Lelieveld, D., van Hoeck, A., Ernst, R. F., Blokzijl, F., Nijman, I. J., Hoogstraat, M., van de Ven, M., Egan, D. A., Zinzalla, V., Moll, J., Boj, S. F., Voest, E. E., Wessels, L., van Diest, P. J., Rottenberg, S., Vries, R. G. J., Cuppen, E., & Clevers, H.
Affiliations: Royal Netherlands Academy of Arts and Sciences (NL)
The Netherlands Cancer Institute (NL)
University Medical Center Utrecht (NL)
Utrecht University (NL)
Boehringer Ingelheim (Austria) (AT)
Oncode Institute (NL)
University of Bern (CH)
Corresponding author: Clevers, Hans
ORCID: Sachs, Norman
Gogola, Ewa
Weeber, Fleur
Begthel, Harry
Ernst, Robert Frans
Blokzijl, Francis
Hoogstraat, Marlous
Boj, Sylvia Fernandez
Voest, Emile Eugene
Wessels, Lodewyk
Rottenberg, Sven
Vries, Robert Gerhardus Jacob
Cuppen, Edwin
Clevers, Hans
Venue: Cell
Publisher: Elsevier BV
Published: 2018-01
Volume: 172
Issue: 1-2
Pages: 373-386.e10
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2017.11.010
OpenAlex: W2773981699
Cited by: 1,973
References: 79
Citations by year: 2026: 219 · 2025: 240 · 2024: 288 · 2023: 251 · 2022: 274 · 2021: 259 · 2020: 238 · 2019: 127 · 2018: 74
FWCI: 53.62
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 375 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Bern Open Repository and Information System (University of Bern) (submittedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion)
Funders: MKMD (114021012)
Netherlands Organization for Scientific Research (91615182, 114021012)
Stand Up to Cancer International Translational Cancer Research Grant
Stichting Vrienden van Hubrecht (2012.010)
Cancer Genomic Center (2014-186)
Boehringer-Ingelheim RCV GmbH & Co KG (141947)
Topics: Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
Keywords: breast cancer, organoid biobank, tumor heterogeneity, metastatic breast cancer, long-term organoid culture, copy number variation, gene expression subtypes, hormone receptor status, HER2 status, in vitro drug testing, xenotransplantation
MeSH terms: Animals, Antineoplastic Agents, Breast Neoplasms, Cells, Cultured, Drug Screening Assays, Antitumor, Female, Humans, Mice, Nude, Organoids, Tissue Banks, Genetic Heterogeneity, Mice, Precision Medicine

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

A Living Biobank of Breast Cancer Organoids Captures Disease Heterogeneity

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks