Conservation of copy number profiles during engraftment and passaging of patient-derived cancer xenografts
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Abstract
Patient-derived xenografts (PDXs) are resected human tumors engrafted into mice for preclinical studies and therapeutic testing. It has been proposed that the mouse host affects tumor evolution during PDX engraftment and propagation, affecting the accuracy of PDX modeling of human cancer. Here, we exhaustively analyze copy number alterations (CNAs) in 1,451 PDX and matched patient tumor (PT) samples from 509 PDX models. CNA inferences based on DNA sequencing and microarray data displayed substantially higher resolution and dynamic range than gene expression-based inferences, and they also showed strong CNA conservation from PTs through late-passage PDXs. CNA recurrence analysis of 130 colorectal and breast PT/PDX-early/PDX-late trios confirmed high-resolution CNA retention. We observed no significant enrichment of cancer-related genes in PDX-specific CNAs across models. Moreover, CNA differences between patient and PDX tumors were comparable to variations in multiregion samples within patients. Our study demonstrates the lack of systematic copy number evolution driven by the PDX mouse host.
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Long-term passage of PDXs in mice can alter tumour behaviour, but strategic use of low-passage lines curbs this mouse-specific drift and remains useful for osteosarcoma biology, precision medicine, and preclinical testing.
“Although prolonged passage in mice can alter the behaviour of tumours maintained as PDXs 227 , strategic use of low-passage PDX lines limits this mouse-specific evolution and is a useful tool in the study of osteosarcoma biology 228 , precision medicine approaches and preclinical validation of therapeutic candidates.”
From Osteosarcoma (2022) · cites this paper as [228]
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Ben‐David, U., Ha, G., Khadka, P., Jin, X., Wong, B., Franke, L., & Golub, T. R. (2016) · Nature Communications · doi:10.1038/ncomms12160 · Cited by 48 · see citing works
Woo, X. Y., Srivastava, A., Graber, J. H., Yadav, V. K., Sarsani, V., Simons, A., Beane, G., Grubb, S. C., Ananda, G., Liu, R., et al. (2019) · BMC Medical Genomics · doi:10.1186/s12920-019-0551-2 · Cited by 48 · see citing works
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Mer, A. S., Ba-Alawi, W., Smirnov, P., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/471227 · Cited by 4 · see citing works
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Beird, H. C., Bielack, S. S., Flanagan, A. M., Gill, J., Heymann, D., Janeway, K. A., Livingston, J. A., Roberts, R. D., Strauss, S. J., & Gorlick, R. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00409-y · Cited by 660 · see citing works
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Self-citationComputational estimation of quality and clinical relevance of cancer cell lines
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Rajan, S., Zaccaria, S., Cannon, M. V., Cam, M., Gross, A. C., Raphael, B. J., & Roberts, R. D. (2021) · doi:10.1101/2021.08.30.458268 · Cited by 33 · see citing works
- Authors
- PDXNET Consortium, Woo, X. Y., EurOPDX Consortium, Giordano, J., Srivastava, A., Zhao, Z.-M., Lloyd, M. W., de Bruijn, R., Suh, Y.-S., Patidar, R., Chen, L., Scherer, S., Bailey, M. H., Yang, C.-H., Cortes-Sanchez, E., Xi, Y., Wang, J., Wickramasinghe, J., Kossenkov, A. V., Rebecca, V. W., Sun, H., Mashl, R. J., Davies, S. R., Jeon, R., Frech, C., Randjelovic, J., Rosains, J., Galimi, F., Bertotti, A., Lafferty, A., O’Farrell, A. C., Modave, E., Lambrechts, D., ter Brugge, P., Serra, V., Marangoni, E., El Botty, R., Kim, H., Kim, J.-I., Yang, H.-K., Lee, C., Dean, D. A., Davis-Dusenbery, B., Evrard, Y. A., Doroshow, J. H., Welm, A. L., Welm, B. E., Lewis, M. T., Fang, B., Roth, J. A., Meric-Bernstam, F., Herlyn, M., Davies, M. A., Ding, L., Li, S., Govindan, R., Isella, C., Moscow, J. A., Trusolino, L., Byrne, A. T., Jonkers, J., Bult, C. J., Medico, E., & Chuang, J. H.
- Affiliations
- The Jackson Laboratory for Genomic Medicine (US)
- Candiolo Cancer Institute (IT)
- Jackson Laboratory (US)
- Seoul National University (KR)
- Frederick National Laboratory for Cancer Research (US)
- University of Utah (US)
- The University of Texas MD Anderson Cancer Center (US)
- The Wistar Institute (US)
- Washington University in St. Louis (US)
- Seven Bridges Genomics (United States) (US)
- Royal College of Surgeons in Ireland (IE)
- VIB-KU Leuven Center for Cancer Biology (BE)
- Vall d'Hebron Institute of Oncology (ES)
- Université Paris Sciences et Lettres (FR)
- Ewha Womans University (KR)
- National Cancer Institute (US)
- Baylor College of Medicine (US)
- National Institutes of Health (US)
- The Netherlands Cancer Institute (NL)
- Corresponding author
- Chuang, Jeffrey H.
- ORCID
- Woo, Xing Yi
- Giordano, Jessica
- Srivastava, Anuj
- Lloyd, Michael W.
- Suh, Yun-Suhk
- Chen, Li
- Scherer, Sandra
- Bailey, Matthew H.
- Cortes-Sanchez, Emilio
- Xi, Yuanxin
- Wang, Jing
- Kossenkov, Andrew V.
- Rebecca, Vito W.
- Sun, Hua
- Mashl, R. Jay
- Davies, Sherri R.
- Frech, Christian
- Galimi, Francesco
- Bertotti, Andrea
- Lafferty, Adam
- O’Farrell, Alice C.
- Modave, Elodie
- Lambrechts, Diether
- Serra, Violeta
- Marangoni, Elisabetta
- Kim, Hyunsoo
- Kim, Jong-Il
- Yang, Han-Kwang
- Lee, Charles
- Dean, Dennis A.
- Evrard, Yvonne A.
- Doroshow, James H.
- Welm, Alana L.
- Welm, Bryan E.
- Lewis, Michael T.
- Fang, Bingliang
- Roth, Jack A.
- Herlyn, Meenhard
- Davies, Michael A.
- Ding, Li
- Li, Shunqiang
- Govindan, Ramaswamy
- Isella, Claudio
- Moscow, Jeffrey A.
- Trusolino, Livio
- Byrne, Annette T.
- Jonkers, Jos
- Bult, Carol J.
- Medico, Enzo
- Chuang, Jeffrey H.
- Venue
- Nature Genetics
- Published
- 2021-01
- Volume
- 53
- Issue
- 1
- Pages
- 86-99
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC7808565
- OpenAlex
- W3121069500
- Cited by
- 190
- References
- 97
- Citations by year
- 2026: 15 · 2025: 23 · 2024: 30 · 2023: 46 · 2022: 41 · 2021: 31 · 2020: 3 · 2014: 1
- FWCI
- 14.92
- Type
- journal article
- Language
- en
- Update notices
- correction (2021-02-19)
- Open access
- hybrid
- doi.org
- Locations
- Nature Genetics (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
- Lirias (submittedVersion, other-oa)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
- eScholarship (California Digital Library) (submittedVersion)
- Lirias (KU Leuven) (submittedVersion)
- Lirias (KU Leuven) (submittedVersion, cc-by)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion, cc-by)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Seoul National University Open Repository (Seoul National University) (submittedVersion)
- Lenus, The Irish Health Repository (Dr Steevens Hospital Library) (submittedVersion, cc-by)
- Funders
- U.S. Department of Health and Human Services (P30CA034196, P30 CA091842, U54 CA224076, HHSN261201400008C, CA125123, HHSN261200800001E, P30-CA042014, HHSN261201500003I, CA091842)
- Breast Cancer Research Foundation
- Eli Lilly and Company
- Pfizer (HHSN261200800001E)
- AstraZeneca
- Foundation for Barnes-Jewish Hospital (P30 CA091842)
- University of Utah (P30 CA042014)
- Huntsman Cancer Institute (P30CA042014)
- Fashion Footwear Association of New York
- Alvin J. Siteman Cancer Center (P30CA091842, CA091842)
- Cancer Research UK (29567, EU H2020, 22795)
- National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC/T001267/1)
- Science Foundation Ireland (13/CDA, 13/CDA/2183, 754923)
- Seoul National University
- Ewha Womans University
- Ministero della Salute (2018-, 2018–2019, 21091)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (18532, 91814643)
- KWF Kankerbestrijding
- Associazione Italiana per la Ricerca sul Cancro (19047, 21091, 20697, 18532, 22795, ID.21091)
- Servier
- Symphogen
- Fundación Fero
- Oncode Institute
- National Institutes of Health (RP170691, #HHSN261200800001E, HHSN261201400008C, HHSN261200800001C, CA- 016672, H2020, HHSN261201500003I, CA091842, NCI U54-CA224083, NCI U54-CA224065, CA-070907, NCI U54-CA233223, CA224083, NCI P30CA042014, NCI U54-CA224070, CA125123, NCI U54-CA233306, NCI U54-CA224076, CA224070)
- University of Texas MD Anderson Cancer Center ((CA016672), CA-070907)
- Horizon 2020 Framework Programme (731105, 754923, EU‐H2020)
- Instituto de Salud Carlos III (CP14/00228, H2020)
- National Human Genome Research Institute (T32HG008962)
- National Cancer Institute (CA-070907, U54CA233223, CA 016672, P01CA114046, U24CA204781, HHSN261200800001E), P50CA196510, 016672, HHSN261201400008C, CA224076, CA125123, P50CA070907, U54CA224065, 731105, HHSN261201500003I, CA091842, CA211199, CA224065, CA233223, U54CA233306, CA196510, CA224070, HHSN261201500003C, RP170691, U54CA224070, R50CA211199, P30CA016672, U54CA224076, U54CA224083, U24CA224067, P30CA042014, P30CA125123, P30CA010815, P30CA091842, P30CA034196)
- H2020 European Research Council (724748)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- patient-derived xenografts, copy number alterations, tumor engraftment, tumor evolution, colorectal cancer, breast cancer, preclinical cancer models
- MeSH terms
- Exome Sequencing, Animals, Humans, Neoplasm Metastasis, Gene Expression Regulation, Neoplastic, Polymorphism, Single Nucleotide, Xenograft Model Antitumor Assays, Databases, Genetic, Mice, DNA Copy Number Variations
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 ›
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