CoChat
Sign Up
Cited by 236

The DOI matches its Crossref record; 37 of the 37 references it cites were found in a registry or an index.

Patient-derived tumor organoids: a new avenue for preclinical research and precision medicine in oncology

Thorel, Lucie, Perréard, Marion, Florent, Romane, Divoux, Jordane, Coffy, Sophia, Vincent, Audrey, Gaggioli, Cédric, Guasch, Géraldine, Gidrol, Xavier, Weiswald, Louis-Bastien, Poulain, Laurent·2024·Experimental & Molecular Medicine
DOI 10.1038/s12276-024-01272-5PMC PMC11297165
Open this paper in CoChat — free account

Abstract

Over the past decade, the emergence of patient-derived tumor organoids (PDTOs) has broadened the repertoire of preclinical models and progressively revolutionized three-dimensional cell culture in oncology. PDTO can be grown from patient tumor samples with high efficiency and faithfully recapitulates the histological and molecular characteristics of the original tumor. Therefore, PDTOs can serve as invaluable tools in oncology research, and their translation to clinical practice is exciting for the future of precision medicine in oncology. In this review, we provide an overview of methods for establishing PDTOs and their various applications in cancer research, starting with basic research and ending with the identification of new targets and preclinical validation of new anticancer compounds and precision medicine. Finally, we highlight the challenges associated with the clinical implementation of PDTO, such as its representativeness, success rate, assay speed, and lack of a tumor microenvironment. Technological developments and autologous cocultures of PDTOs and stromal cells are currently ongoing to meet these challenges and optimally exploit the full potential of these models. The use of PDTOs as standard tools in clinical oncology could lead to a new era of precision oncology in the coming decade.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s12276-024-01272-5

Cites

37 of 37 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

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

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Show all 37 references

Research works printed but not linked: 162

  1. Scherer, W. F., Syverton, J. T. & Gey, G. O. Studies on the propagation in vitro of poliomyelitis viruses. J. Exp. Med. 97, 695–710 (1953). · DOI · Paper page
  2. Borrell, B. How accurate are cancer cell lines? Nature 463, 858–858 (2010). · DOI
  3. Sutherland, R. M., Inch, W. R., McCredie, J. A. & Kruuv, J. A multi-component radiation survival curve using an in vitro tumour model. Int J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 18, 491–495 (1970). · DOI
  4. Weiswald, L.-B., Bellet, D. & Dangles-Marie, V. Spherical cancer models in tumor biology. Neoplasia 17, 1–15 (2015). · DOI
  5. Freeman, A. E. & Hoffman, R. M. In vivo-like growth of human tumors in vitro. Proc. Natl Acad. Sci. USA 83, 2694–2698 (1986). · DOI
  6. Bjerkvig, R., Tønnesen, A., Laerum, O. D. & Backlund, E. O. Multicellular tumor spheroids from human gliomas maintained in organ culture. J. Neurosurg. 72, 463–475 (1990). · DOI
  7. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 3983–3988 (2003). · DOI
  8. Singh, S. K. et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63, 5821–5828 (2003).
  9. Weiswald, L.-B. et al. Newly characterised ex vivo colospheres as a three-dimensional colon cancer cell model of tumour aggressiveness. Br. J. Cancer 101, 473–482 (2009). · DOI
  10. Foo, M. A. et al. Clinical translation of patient-derived tumour organoids- bottlenecks and strategies. Biomark. Res. 10, 10 (2022). · DOI
  11. Driehuis, E., Kretzschmar, K. & Clevers, H. Establishment of patient-derived cancer organoids for drug-screening applications. Nat. Protoc. 15, 3380–3409 (2020). · DOI
  12. Xu, H. et al. Organoid technology and applications in cancer research. J. Hematol. Oncol. 11, 116 (2018). · DOI
  13. Barbet, V. & Broutier, L. Future Match Making: When Pediatric Oncology Meets Organoid Technology. Front. Cell Dev. Biol. 9, 674219 (2021). · DOI
  14. DeRose, Y. S. et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat. Med. 17, 1514–1520 (2011). · DOI
  15. Kopper, O. et al. An organoid platform for ovarian cancer captures intra- and interpatient heterogeneity. Nat. Med. 25, 838–849 (2019). · DOI · Paper page
  16. Dolega, M. E., Abeille, F., Picollet-D’hahan, N. & Gidrol, X. Controlled 3D culture in Matrigel microbeads to analyze clonal acinar development. Biomaterials 52, 347–357 (2015). · DOI · Paper page
  17. Passaniti, A., Kleinman, H. K. & Martin, G. R. Matrigel: history/background, uses, and future applications. J. Cell Commun. Signal 16, 621–626 (2022). · DOI
  18. Sachs, N., Tsukamoto, Y., Kujala, P., Peters, P. J. & Clevers, H. Intestinal epithelial organoids fuse to form self-organizing tubes in floating collagen gels. Development 144, 1107–1112 (2017). · DOI
  19. Sokol, E. S. et al. Growth of human breast tissues from patient cells in 3D hydrogel scaffolds. Breast Cancer Res. 18, 19 (2016). · DOI
  20. Giobbe, G. G. et al. Extracellular matrix hydrogel derived from decellularized tissues enables endodermal organoid culture. Nat. Commun. 10, 5658 (2019). · DOI · Paper page
  21. Gjorevski, N. & Lutolf, M. P. Synthesis and characterization of well-defined hydrogel matrices and their application to intestinal stem cell and organoid culture. Nat. Protoc. 12, 2263–2274 (2017). · DOI
  22. Lancaster, M. A. et al. Guided self-organization and cortical plate formation in human brain organoids. Nat. Biotechnol. 35, 659–666 (2017). · DOI · Paper page
  23. Patel, S., Alam, A., Pant, R. & Chattopadhyay, S. Wnt Signaling and Its Significance Within the Tumor Microenvironment: Novel Therapeutic Insights. Front. Immunol. 10, 2872 (2019). · DOI
  24. Fujii, M. et al. A Colorectal Tumor Organoid Library Demonstrates Progressive Loss of Niche Factor Requirements during Tumorigenesis. Cell Stem Cell 18, 827–838 (2016). · DOI · Paper page
  25. Verissimo, C. S. et al. Targeting mutant RAS in patient-derived colorectal cancer organoids by combinatorial drug screening. Elife 5, e18489 (2016). · DOI · Paper page
  26. Li, X., Ootani, A. & Kuo, C. An Air-Liquid Interface Culture System for 3D Organoid Culture of Diverse Primary Gastrointestinal Tissues. Methods Mol. Biol. 1422, 33–40 (2016). · DOI
  27. Co, J. Y., Margalef-Català, M., Monack, D. M. & Amieva, M. R. Controlling the polarity of human gastrointestinal organoids to investigate epithelial biology and infectious diseases. Nat. Protoc. 16, 5171–5192 (2021). · DOI
  28. Jacob, F. et al. A Patient-Derived Glioblastoma Organoid Model and Biobank Recapitulates Inter- and Intra-tumoral Heterogeneity. Cell 180, 188–204.e22 (2020). · DOI · Paper page
  29. Bürtin, F. et al. Creation and Maintenance of a Living Biobank - How We Do It. J. Vis. Exp. https://doi.org/10.3791/62065. (2021). · DOI
  30. Hoare, O. et al. Exploring the Complementarity of Pancreatic Ductal Adenocarcinoma Preclinical Models. Cancers 13, 2473 (2021). · DOI
  31. Derouet, M. F. et al. Towards personalized induction therapy for esophageal adenocarcinoma: organoids derived from endoscopic biopsy recapitulate the pre-treatment tumor. Sci. Rep. 10, 14514 (2020). · DOI
  32. Gorski, J. W. et al. Utilizing Patient-Derived Epithelial Ovarian Cancer Tumor Organoids to Predict Carboplatin Resistance. Biomedicines 9, 1021 (2021). · DOI
  33. Liu, H.-D., Xia, B.-R., Jin, M.-Z. & Lou, G. Organoid of ovarian cancer: genomic analysis and drug screening. Clin. Transl. Oncol. 22, 1240–1251 (2020). · DOI
  34. Becker, L. et al. Data-Driven Identification of Biomarkers for In Situ Monitoring of Drug Treatment in Bladder Cancer Organoids. Int. J. Mol. Sci. 23, 6956 (2022). · DOI
  35. Spiller, E. R. et al. Imaging-Based Machine Learning Analysis of Patient-Derived Tumor Organoid Drug Response. Front. Oncol. 11, 771173 (2021). · DOI
  36. Sharick, J. T. et al. Metabolic Heterogeneity in Patient Tumor-Derived Organoids by Primary Site and Drug Treatment. Front. Oncol. 10, 553 (2020). · DOI
  37. Neef, S. K. et al. Metabolic Drug Response Phenotyping in Colorectal Cancer Organoids by LC-QTOF-MS. Metabolites 10, 494 (2020). · DOI
  38. Yao, Y. et al. Patient-Derived Organoids Predict Chemoradiation Responses of Locally Advanced Rectal Cancer. Cell Stem Cell 26, 17–26.e6 (2020). · DOI · Paper page
  39. Scognamiglio, G. et al. Patient-derived organoids as a potential model to predict response to PD-1/PD-L1 checkpoint inhibitors. Br. J. Cancer 121, 979–982 (2019). · DOI
  40. Dekkers, J. F. et al. Modeling Breast Cancer Using CRISPR-Cas9-Mediated Engineering of Human Breast Organoids. J. Natl Cancer Inst. 112, 540–544 (2020). · DOI
  41. Seino, T. et al. Human Pancreatic Tumor Organoids Reveal Loss of Stem Cell Niche Factor Dependence during Disease Progression. Cell Stem Cell 22, 454–467.e6 (2018). · DOI · Paper page
  42. Hu, T. et al. Metabolic Rewiring by Loss of Sirt5 Promotes Kras-Induced Pancreatic Cancer Progression. Gastroenterology 161, 1584–1600 (2021). · DOI
  43. Li, F. et al. Identification of ARGLU1 as a potential therapeutic target for gastric cancer based on genome-wide functional screening data. EBioMedicine 69, 103436 (2021). · DOI
  44. Picollet-D’hahan, N., Dolega, M. E., Freida, D., Martin, D. K. & Gidrol, X. Deciphering Cell Intrinsic Properties: A Key Issue for Robust Organoid Production. Trends Biotechnol. 35, 1035–1048 (2017). · DOI
  45. Germain, N. et al. Lipid Metabolism and Resistance to Anticancer Treatment. Biology 9, 474 (2020). · DOI
  46. Strauss, J. & Figg, W. D. Epigenetic approaches to overcoming chemotherapy resistance. Lancet Oncol. 16, 1013–1015 (2015). · DOI
  47. El Amrani, M. et al. Gemcitabine-induced epithelial-mesenchymal transition-like changes sustain chemoresistance of pancreatic cancer cells of mesenchymal-like phenotype. Mol. Carcinog. 58, 1985–1997 (2019). · DOI
  48. Fernandes, M., Jamme, P., Cortot, A. B., Kherrouche, Z. & Tulasne, D. When the MET receptor kicks in to resist targeted therapies. Oncogene 40, 4061–4078 (2021). · DOI
  49. Sundar, S. J. et al. Three-dimensional organoid culture unveils resistance to clinical therapies in adult and pediatric glioblastoma. Transl. Oncol. 15, 101251 (2021). · DOI
  50. Farshadi, E. A. et al. Organoids Derived from Neoadjuvant FOLFIRINOX Patients Recapitulate Therapy Resistance in Pancreatic Ductal Adenocarcinoma. Clin. Cancer Res. 27, 6602–6612 (2021). · DOI
  51. Huang, L. et al. PDX-derived organoids model in vivo drug response and secrete biomarkers. JCI Insight 5, e135544 (2020). · DOI
  52. Hadj Bachir, E. et al. A new pancreatic adenocarcinoma-derived organoid model of acquired chemoresistance to FOLFIRINOX: First insight of the underlying mechanisms. Biol. Cell 114, 32–55 (2022). · DOI
  53. Driehuis, E. et al. Pancreatic cancer organoids recapitulate disease and allow personalized drug screening. Proc. Natl Acad. Sci. 116, 26580–26590 (2019). · DOI
  54. Tan, P. et al. SRT1720 inhibits the growth of bladder cancer in organoids and murine models through the SIRT1-HIF axis. Oncogene 40, 6081–6092 (2021). · DOI
  55. Yan, H. H. N. et al. A Comprehensive Human Gastric Cancer Organoid Biobank Captures Tumor Subtype Heterogeneity and Enables Therapeutic Screening. Cell Stem Cell 23, 882–897.e11 (2018). · DOI · Paper page
  56. Calandrini, C. et al. Organoid-based drug screening reveals neddylation as therapeutic target for malignant rhabdoid tumors. Cell Rep. 36, 109568 (2021). · DOI
  57. Vernon, M. et al. Functional miRNA Screening Identifies Wide-ranging Antitumor Properties of miR-3622b-5p and Reveals a New Therapeutic Combination Strategy in Ovarian Tumor Organoids. Mol. Cancer Therapeutics 19, 1506–1519 (2020). · DOI
  58. Florent, R. et al. Bim, Puma and Noxa upregulation by Naftopidil sensitizes ovarian cancer to the BH3-mimetic ABT-737 and the MEK inhibitor Trametinib. Cell Death Dis. 11, 1–16 (2020). · DOI
  59. Wambecke, A. et al. The lncRNA ‘UCA1’ modulates the response to chemotherapy of ovarian cancer through direct binding to miR‐27a‐5p and control of UBE2N levels. Mol. Oncol. 15, 3659–3678 (2021). · DOI
  60. Garvey, C. M. et al. Anti-EGFR Therapy Induces EGF Secretion by Cancer-Associated Fibroblasts to Confer Colorectal Cancer Chemoresistance. Cancers 12, 1393 (2020). · DOI
  61. Millen, R. et al. Patient-derived head and neck cancer organoids allow treatment stratification and serve as a tool for biomarker validation and identification. Medicine 4, 290–310.e12 (2023). · DOI
  62. Chen, G. et al. Colorectal cancer organoid models uncover oxaliplatin-resistant mechanisms at single cell resolution. Cell Oncol. 45, 1155–1167 (2022). · DOI
  63. Shi, X. et al. Integrated profiling of human pancreatic cancer organoids reveals chromatin accessibility features associated with drug sensitivity. Nat. Commun. 13, 2169 (2022). · DOI
  64. Braun, L. M. et al. Metabolic Profiling of Early and Late Recurrent Pancreatic Ductal Adenocarcinoma Using Patient-Derived Organoid Cultures. Cancers 12, 1440 (2020). · DOI
  65. Kong, J. et al. Network-based machine learning in colorectal and bladder organoid models predicts anti-cancer drug efficacy in patients. Nat. Commun. 11, 5485 (2020). · DOI
  66. Ancevski Hunter, K., Socinski, M. A. & Villaruz, L. C. PD-L1 Testing in Guiding Patient Selection for PD-1/PD-L1 Inhibitor Therapy in Lung Cancer. Mol. Diagn. Ther. 22, 1–10 (2018). · DOI
  67. Letai, A., Bhola, P. & Welm, A. L. Functional precision oncology: Testing tumors with drugs to identify vulnerabilities and novel combinations. Cancer Cell 40, 26–35 (2022). · DOI
  68. Mirza, M. R. et al. Niraparib Maintenance Therapy in Platinum-Sensitive, Recurrent Ovarian Cancer. N. Engl. J. Med. 375, 2154–2164 (2016). · DOI
  69. Federici, G. & Soddu, S. Variants of uncertain significance in the era of high-throughput genome sequencing: a lesson from breast and ovary cancers. J. Exp. Clin. Cancer Res. 39, 46 (2020). · DOI
  70. Nicolle, R. et al. Relevance of biopsy-derived pancreatic organoids in the development of efficient transcriptomic signatures to predict adjuvant chemosensitivity in pancreatic cancer. Transl. Oncol. 16, 101315 (2022). · DOI
  71. Verduin, M., Hoeben, A., De Ruysscher, D. & Vooijs, M. Patient-Derived Cancer Organoids as Predictors of Treatment Response. Front. Oncol. 11, 641980 (2021). · DOI
  72. Wensink, G. E. et al. Patient-derived organoids as a predictive biomarker for treatment response in cancer patients. NPJ Precis Oncol. 5, 30 (2021). · DOI · Paper page
  73. Tsukamoto, Y. et al. Enhanced phosphorylation of c-Jun by cisplatin treatment as a potential predictive biomarker for cisplatin response in combination with patient-derived tumor organoids. Lab. Invest. 102, 1355–1366 (2022). · DOI
  74. Beutel, A. K. et al. A Prospective Feasibility Trial to Challenge Patient–Derived Pancreatic Cancer Organoids in Predicting Treatment Response. Cancers 13, 2539 (2021). · DOI
  75. Park, M. et al. A Patient-Derived Organoid-Based Radiosensitivity Model for the Prediction of Radiation Responses in Patients with Rectal Cancer. Cancers 13, 3760 (2021). · DOI
  76. Driehuis, E. et al. Oral Mucosal Organoids as a Potential Platform for Personalized Cancer Therapy. Cancer Discov. 9, 852–871 (2019). · DOI · Paper page
  77. Mauri, G. et al. Empowering Clinical Decision Making in Oligometastatic Colorectal Cancer: The Potential Role of Drug Screening of Patient-Derived Organoids. JCO Precis. Oncol. 5, PO.21.00143 (2021).
  78. Buyse, M. et al. Progression-free survival is a surrogate for survival in advanced colorectal cancer. J. Clin. Oncol. 25, 5218–5224 (2007). · DOI
  79. Ooft, S. N. et al. Prospective experimental treatment of colorectal cancer patients based on organoid drug responses. ESMO Open 6, 100103 (2021). · DOI
  80. Liu, Y. et al. Combining Organoid Models with Next-Generation Sequencing to Reveal Tumor Heterogeneity and Predict Therapeutic Response in Breast Cancer. J. Oncol. 2022, 9390912 (2022).
  81. Kim, M. et al. Patient-derived lung cancer organoids as in vitro cancer models for therapeutic screening. Nat. Commun. 10, 3991 (2019). · DOI · Paper page
  82. Dijkstra, K. K. et al. Challenges in Establishing Pure Lung Cancer Organoids Limit Their Utility for Personalized Medicine. Cell Rep. 31, 107588 (2020). · DOI · Paper page
  83. Wallaschek, N. et al. Establishing Pure Cancer Organoid Cultures: Identification, Selection and Verification of Cancer Phenotypes and Genotypes. J. Mol. Biol. 431, 2884–2893 (2019). · DOI
  84. Colella, G. et al. Sarcoma Spheroids and Organoids-Promising Tools in the Era of Personalized Medicine. Int J. Mol. Sci. 19, 615 (2018). · DOI
  85. Majumder, B. et al. Predicting clinical response to anticancer drugs using an ex vivo platform that captures tumour heterogeneity. Nat. Commun. 6, 6169 (2015). · DOI
  86. Heo, J. H., Kang, D., Seo, S. J. & Jin, Y. Engineering the Extracellular Matrix for Organoid Culture. Int J. Stem Cells 15, 60–69 (2022). · DOI
  87. Xie, Z., Wang, L. & Zhang, Y. Advances in Organoid Culture Research. Glob. Med. Genet 9, 268–276 (2022). · DOI
  88. Ding, S. et al. Patient-derived micro-organospheres enable clinical precision oncology. Cell Stem Cell 29, 905–917.e6 (2022). · DOI · Paper page
  89. Phan, N. et al. A simple high-throughput approach identifies actionable drug sensitivities in patient-derived tumor organoids. Commun. Biol. 2, 78 (2019). · DOI · Paper page
  90. Kim, S. K., Kim, Y. H., Park, S. & Cho, S.-W. Organoid engineering with microfluidics and biomaterials for liver, lung disease, and cancer modeling. Acta Biomater. 132, 37–51 (2021). · DOI
  91. Larsen, B. M., Cancino, A., Shaxted, J. M. & Salahudeen, A. A. Protocol for drug screening of patient-derived tumor organoids using high-content fluorescent imaging. STAR Protoc. 3, 101407 (2022). · DOI
  92. Wang, J. et al. Patient-Derived Tumor Organoids: New Progress and Opportunities to Facilitate Precision Cancer Immunotherapy. Front. Oncol. 12, 872531 (2022). · DOI
  93. Liu, L., Yu, L., Li, Z., Li, W. & Huang, W. Patient-derived organoid (PDO) platforms to facilitate clinical decision making. J. Transl. Med. 19, 40 (2021). · DOI
  94. Qu, J., Kalyani, F. S., Liu, L., Cheng, T. & Chen, L. Tumor organoids: synergistic applications, current challenges, and future prospects in cancer therapy. Cancer Commun. 41, 1331–1353 (2021). · DOI
  95. Fan, T. W. et al. Innate immune activation by checkpoint inhibition in human patient-derived lung cancer tissues. Elife 10, e69578 (2021). · DOI
  96. Martin, S. Z. et al. Ex vivo tissue slice culture system to measure drug-response rates of hepatic metastatic colorectal cancer. BMC Cancer 19, 1030 (2019). · DOI
  97. Saleh, R., Toor, S. M., Al-Ali, D., Sasidharan Nair, V. & Elkord, E. Blockade of PD-1, PD-L1, and TIM-3 Altered Distinct Immune- and Cancer-Related Signaling Pathways in the Transcriptome of Human Breast Cancer Explants. Genes 11, 703 (2020). · DOI
  98. Wan, C. et al. Enhanced Efficacy of Simultaneous PD-1 and PD-L1 Immune Checkpoint Blockade in High-Grade Serous Ovarian Cancer. Cancer Res. 81, 158–173 (2021). · DOI
  99. Ao, Z. et al. Rapid Profiling of Tumor-Immune Interaction Using Acoustically Assembled Patient-Derived Cell Clusters. Adv. Sci. 9, e2201478 (2022). · DOI
  100. Knochelmann, H. M. et al. Modeling ex vivo tumor-infiltrating lymphocyte expansion from established solid malignancies. Oncoimmunology 10, 1959101 (2021). · DOI
  101. Bonnereau, J. et al. Autologous T cell responses to primary human colorectal cancer spheroids are enhanced by ectonucleotidase inhibition. Gut 72, 699–709 (2023). · DOI
  102. Hammoudi, N. et al. Autologous organoid co-culture model reveals T cell-driven epithelial cell death in Crohn’s Disease. Front. Immunol. 13, 1008456 (2022). · DOI
  103. Kong, J. C. H. et al. Tumor-Infiltrating Lymphocyte Function Predicts Response to Neoadjuvant Chemoradiotherapy in Locally Advanced Rectal Cancer. JCO Precis. Oncol. 2, 1–15 (2018). · DOI
  104. Nozaki, K. et al. Co-culture with intestinal epithelial organoids allows efficient expansion and motility analysis of intraepithelial lymphocytes. J. Gastroenterol. 51, 206–213 (2016). · DOI
  105. Votanopoulos, K. I. et al. Model of Patient-Specific Immune-Enhanced Organoids for Immunotherapy Screening: Feasibility Study. Ann. Surg. Oncol. 27, 1956–1967 (2020). · DOI
  106. Forsythe, S. D. et al. Organoid Platform in Preclinical Investigation of Personalized Immunotherapy Efficacy in Appendiceal Cancer: Feasibility Study. Clin. Cancer Res. 27, 5141–5150 (2021). · DOI
  107. Forsythe, S. D. et al. Application of immune enhanced organoids in modeling personalized Merkel cell carcinoma research. Sci. Rep. 12, 13865 (2022). · DOI
  108. Holokai, L. et al. Murine- and Human-Derived Autologous Organoid/Immune Cell Co-Cultures as Pre-Clinical Models of Pancreatic Ductal Adenocarcinoma. Cancers 12, 3816 (2020). · DOI
  109. Tsai, S. et al. Development of primary human pancreatic cancer organoids, matched stromal and immune cells and 3D tumor microenvironment models. BMC Cancer 18, 335 (2018). · DOI · Paper page
  110. Chalabi, M. et al. Neoadjuvant immunotherapy leads to pathological responses in MMR-proficient and MMR-deficient early-stage colon cancers. Nat. Med. 26, 566–576 (2020). · DOI · Paper page
  111. Cattaneo, C. M. et al. Tumor organoid-T-cell coculture systems. Nat. Protoc. 15, 15–39 (2020). · DOI · Paper page
  112. Clinton, J. & McWilliams-Koeppen, P. Initiation, Expansion, and Cryopreservation of Human Primary Tissue-Derived Normal and Diseased Organoids in Embedded Three-Dimensional Culture. Curr. Protoc. Cell Biol. 82, e66 (2019). · DOI
  113. Zhao, H., Jiang, E. & Shang, Z. 3D Co-culture of Cancer-Associated Fibroblast with Oral Cancer Organoids. J. Dent. Res. 100, 201–208 (2021). · DOI
  114. Chen, X. et al. Phenotype transition of fibroblasts incorporated into patient-derived oral carcinoma organoids. Oral. Dis. 29, 913–922 (2023). · DOI
  115. Chen, S. et al. Cancer-associated fibroblasts suppress SOX2-induced dysplasia in a lung squamous cancer coculture. Proc. Natl Acad. Sci. USA 115, E11671–E11680 (2018). · DOI
  116. Liu, J. et al. Cancer-Associated Fibroblasts Provide a Stromal Niche for Liver Cancer Organoids That Confers Trophic Effects and Therapy Resistance. Cell Mol. Gastroenterol. Hepatol. 11, 407–431 (2021). · DOI
  117. Truelsen, S. L. B. et al. The cancer angiogenesis co-culture assay: In vitro quantification of the angiogenic potential of tumoroids. PLoS One 16, e0253258 (2021). · DOI
  118. Arslan, U. et al. Vascularized hiPSC-derived 3D cardiac microtissue on chip. Stem Cell Rep. 18, 1394–1404 (2023). · DOI · Paper page
  119. Ugrinic, M. et al. Fabrication of high aspect ratio microfluidic devices for long term in vitro culture of 3D tumor models. Microelectronic Eng. 267–268, 111898 (2023). · DOI
  120. Russell, T. et al. Cortical spheroid on perfusable microvascular network in a microfluidic device. Plos One 18, 1–14 (2023). · DOI
  121. Lee, S.-R. et al. U-IMPACT: a universal 3D microfluidic cell culture platform. Microsyst. Nanoeng. 8, 126 (2022). · DOI
  122. Cai, H. et al. Trapping cell spheroids and organoids using digital acoustofluidics. Biofabrication 12, 035025 (2020). · DOI
  123. Quintard, C. et al. Microfluidic device integrating a network of hyper-elastic valves for automated glucose stimulation and insulin secretion collection from a single pancreatic islet. Biosens. Bioelectron. 202, 113967 (2022). · DOI
  124. Wang, X. et al. A Tumor‐Organoid‐Based Precision Medicine Platform for the Prediction of Drug Sensitivity of Colorectal Cancer. Adv. Therapeutics 5, 2200093 (2022). · DOI
  125. Schuster, B. et al. Automated microfluidic platform for dynamic and combinatorial drug screening of tumor organoids. Nat. Commun. 11, 5271 (2020). · DOI · Paper page
  126. Pinho, D., Santos, D., Vila, A. & Carvalho, S. Establishment of colorectal cancer organoids in microfluidic-based system. Micromachines 12, 497 (2021). · DOI
  127. Cavarzerani, E., Caligiuri, I., Bartoletti, M., Canzonieri, V. & Rizzolio, F. 3D dynamic cultures of HGSOC organoids to model innovative and standard therapies. Front. Bioeng. Biotechnol. 11, 1–13 (2023). · DOI
  128. Hachey, S. J. et al. A human vascularized microtumor model of patient-derived colorectal cancer recapitulates clinical disease. Transl. Res. 255, 97–108 (2023). · DOI
  129. Rajasekar, S. et al. IFlowPlate—A Customized 384‐Well Plate for the Culture of Perfusable Vascularized Colon Organoids. Adva. Mater. 32, e2002974 (2020). · DOI
  130. Palikuqi, B. et al. Adaptable haemodynamic endothelial cells for organogenesis and tumorigenesis. Nature 585, 426–432 (2020). · DOI · Paper page
  131. Bussooa, A. et al. Real-time monitoring of oxygen levels within thermoplastic Organ-on-Chip devices. Biosens. Bioelectron. X 11, 4–11 (2022).
  132. Dornhof, J. et al. Microfluidic organ-on-chip system for multi-analyte monitoring of metabolites in 3D cell cultures. Lab Chip 22, 225–239 (2022). · DOI
  133. Votanopoulos, K. I. et al. Appendiceal Cancer Patient-Specific Tumor Organoid Model for Predicting Chemotherapy Efficacy Prior to Initiation of Treatment: A Feasibility Study. Ann. Surg. Oncol. 26, 139–147 (2019). · DOI
  134. Saito, Y. et al. Establishment of Patient-Derived Organoids and Drug Screening for Biliary Tract Carcinoma. Cell Rep. 27, 1265–1276.e4 (2019). · DOI
  135. Wang, Z. et al. Establishment and drug screening of patient-derived extrahepatic biliary tract carcinoma organoids. Cancer Cell Int. 21, 519 (2021). · DOI
  136. Schütte, M. et al. Molecular dissection of colorectal cancer in pre-clinical models identifies biomarkers predicting sensitivity to EGFR inhibitors. Nat. Commun. 8, 14262 (2017). · DOI
  137. Buzzelli, J. N., Ouaret, D., Brown, G., Allen, P. D. & Muschel, R. J. Colorectal cancer liver metastases organoids retain characteristics of original tumor and acquire chemotherapy resistance. Stem Cell Res. 27, 109–120 (2018). · DOI
  138. Narasimhan, V. et al. Medium-throughput Drug Screening of Patient-derived Organoids from Colorectal Peritoneal Metastases to Direct Personalized Therapy. Clin. Cancer Res. 26, 3662–3670 (2020). · DOI
  139. Nanki, K. et al. Divergent Routes toward Wnt and R-spondin Niche Independency during Human Gastric Carcinogenesis. Cell 174, 856–869.e17 (2018). · DOI
  140. Li, J. et al. Malignant ascites-derived organoid (MADO) cultures for gastric cancer in vitro modelling and drug screening. J. Cancer Res. Clin. Oncol. 145, 2637–2647 (2019). · DOI
  141. D’Agosto, S. et al. Long-term organoid culture of a small intestinal neuroendocrine tumor. Front. Endocrinol. 14, 999792 (2023). · DOI
  142. Dijkstra, K. K. et al. Patient-Derived Organoid Models of Human Neuroendocrine Carcinoma. Front. Endocrinol. 12, 627819 (2021). · DOI
  143. Beato, F. et al. Establishing a Living Biobank of Patient-Derived Organoids of Intraductal Papillary Mucinous Neoplasms of the Pancreas. Lab. Invest. 101, 204–217 (2021). · DOI
  144. Mazzucchelli, S. et al. Establishment and Morphological Characterization of Patient-Derived Organoids from Breast Cancer. Biol. Proced. Online 21, 12 (2019). · DOI
  145. Boretto, M. et al. Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat. Cell Biol. 21, 1041–1051 (2019). · DOI
  146. Tanaka, N. et al. Head and neck cancer organoids established by modification of the CTOS method can be used to predict in vivo drug sensitivity. Oral. Oncol. 87, 49–57 (2018). · DOI
  147. Kijima, T. et al. Three-Dimensional Organoids Reveal Therapy Resistance of Esophageal and Oropharyngeal Squamous Cell Carcinoma Cells. Cell Mol. Gastroenterol. Hepatol. 7, 73–91 (2019). · DOI
  148. Karakasheva, T. A. et al. Generation and characterization of patient-derived esophageal cancer organoids. Curr. Protoc. Stem Cell Biol. 53, e109 (2020). · DOI
  149. Wang, B. et al. An organoid library of salivary gland tumors reveals subtype-specific characteristics and biomarkers. J. Exp. Clin. Cancer Res. 41, 350 (2022). · DOI
  150. Lassche, G. et al. Development and characterization of patient-derived salivary gland cancer organoid cultures. Oral. Oncol. 135, 106186 (2022). · DOI
  151. Sondorp, L. H. J. et al. Patient-Derived Papillary Thyroid Cancer Organoids for Radioactive Iodine Refractory Screening. Cancers 12, 3212 (2020). · DOI
  152. Yang, H. et al. Establishment of papillary thyroid cancer organoid lines from clinical specimens. Front. Endocrinol. 14, 1140888 (2023). · DOI
  153. Jiang, Y. et al. Patient-derived bladder cancer organoid model to predict sensitivity and feasibility of tailored precision therapy. Curr. Urol. 17, 221–228 (2023). · DOI
  154. Bolck, H. A. et al. Tracing Clonal Dynamics Reveals that Two- and Three-dimensional Patient-derived Cell Models Capture Tumor Heterogeneity of Clear Cell Renal Cell Carcinoma. Eur. Urol. Focus 7, 152–162 (2021). · DOI
  155. Li, Z. et al. Patient‐derived renal cell carcinoma organoids for personalized cancer therapy. Clin. Transl. Med. 12, e970 (2022). · DOI
  156. Puca, L. et al. Patient derived organoids to model rare prostate cancer phenotypes. Nat. Commun. 9, 2404 (2018). · DOI
  157. Mazzocchi, A. R., Rajan, S. A. P., Votanopoulos, K. I., Hall, A. R. & Skardal, A. In vitro patient-derived 3D mesothelioma tumor organoids facilitate patient-centric therapeutic screening. Sci. Rep. 8, 2886 (2018). · DOI
  158. Fang, X. et al. Organoids derived from patients provide a new opportunity for research and individualized treatment of malignant peritoneal mesothelioma. Mol. Cancer 23, 12 (2024). · DOI
  159. Ou, L. et al. Patient-derived melanoma organoid models facilitate the assessment of immunotherapies. EBioMedicine 92, 104614 (2023). · DOI
  160. Sun, L. et al. A human mucosal melanoma organoid platform for modeling tumor heterogeneity and exploring immunotherapy combination options. Sci. Adv. 9, eadg6686 (2023). · DOI
  161. Thorel, L. et al. Patient-derived tumor organoids (or tumoroid), a growing preclinical model for oncology. Med. Sci. (Paris) 38, 880–887 (2022). · DOI
  162. Perréard, M. et al. Patient-derived tumor organoids (or tumoroid) as valuable precision medicine tools. Med. Sci. (Paris) 38, 888–895 (2022). · DOI

Cited by

Sorted by citations

See all 236

Metadata

Authors
Thorel, L., Perréard, M., Florent, R., Divoux, J., Coffy, S., Vincent, A., Gaggioli, C., Guasch, G., Gidrol, X., Weiswald, L.-B., & Poulain, L.
Venue
Experimental & Molecular Medicine
Publisher
Springer Science and Business Media LLC
Published
2024-07-01
Volume
56
Issue
7
Pages
1531-1551
ISSN
2092-6413
DOI
10.1038/s12276-024-01272-5
PMC
PMC11297165
Cited by
236
References
37
Language
en
Licence

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