Spatial genomics maps the structure, nature and evolution of cancer clones.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Nov 2022
Historique:
received: 21 04 2021
accepted: 07 10 2022
pubmed: 10 11 2022
medline: 22 11 2022
entrez: 9 11 2022
Statut: ppublish

Résumé

Genome sequencing of cancers often reveals mosaics of different subclones present in the same tumour

Identifiants

pubmed: 36352222
doi: 10.1038/s41586-022-05425-2
pii: 10.1038/s41586-022-05425-2
pmc: PMC9668746
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

594-602

Subventions

Organisme : NCI NIH HHS
ID : U54 CA225088
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA168504
Pays : United States
Organisme : Wellcome Trust
ID : 108413/A/15/D
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 214584/Z/18/Z
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2022. The Author(s).

Références

Gerstung, M. et al. The evolutionary history of 2,658 cancers. Nature 578, 122–128 (2020).
pubmed: 32025013 pmcid: 7054212 doi: 10.1038/s41586-019-1907-7
Andor, N. et al. Pan-cancer analysis of the extent and consequences of intratumor heterogeneity. Nat. Med. 22, 105–113 (2016).
pubmed: 26618723 doi: 10.1038/nm.3984
Yates, L. R. et al. Subclonal diversification of primary breast cancer revealed by multiregion sequencing. Nat. Med. 21, 751–759 (2015).
pubmed: 26099045 pmcid: 4500826 doi: 10.1038/nm.3886
Greaves, M. & Maley, C. C. Clonal evolution in cancer. Nature 481, 306–313 (2012).
pubmed: 22258609 pmcid: 3367003 doi: 10.1038/nature10762
McGranahan, N. & Swanton, C. Clonal heterogeneity and tumor evolution: past, present, and the future. Cell 168, 613–628 (2017).
pubmed: 28187284 doi: 10.1016/j.cell.2017.01.018
Nowell, P. C. The clonal evolution of tumor cell populations. Science 194, 23–28 (1976).
pubmed: 959840 doi: 10.1126/science.959840
Dentro, S. C. et al. Characterizing genetic intra-tumor heterogeneity across 2,658 human cancer genomes. Cell 184, 2239–2254.e39 (2021).
pubmed: 33831375 pmcid: 8054914 doi: 10.1016/j.cell.2021.03.009
Nik-Zainal, S. et al. The life history of 21 breast cancers. Cell 149, 994–1007 (2012).
pubmed: 22608083 pmcid: 3428864 doi: 10.1016/j.cell.2012.04.023
Gaglia, G. et al. Temporal and spatial topography of cell proliferation in cancer. Nat. Cell Biol. 24, 316–326 (2022).
pubmed: 35292783 pmcid: 8959396 doi: 10.1038/s41556-022-00860-9
Risom, T. et al. Transition to invasive breast cancer is associated with progressive changes in the structure and composition of tumor stroma. Cell 185, 299–310.e18 (2022).
pubmed: 35063072 pmcid: 8792442 doi: 10.1016/j.cell.2021.12.023
Dhainaut, M. et al. Spatial CRISPR genomics identifies regulators of the tumor microenvironment. Cell 185, 1223–1239.e20 (2022).
pubmed: 35290801 doi: 10.1016/j.cell.2022.02.015
Yates, L. R. et al. Genomic evolution of breast cancer metastasis and relapse. Cancer Cell 32, 169–184.e7 (2017).
pubmed: 28810143 pmcid: 5559645 doi: 10.1016/j.ccell.2017.07.005
Maley, C. C. et al. Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nat. Genet. 38, 468–473 (2006).
pubmed: 16565718 doi: 10.1038/ng1768
Jamal-Hanjani, M. et al. Tracking the evolution of non–small-cell lung cancer. N. Engl. J. Med. 376, 2109–2121 (2017).
pubmed: 28445112 doi: 10.1056/NEJMoa1616288
Janiszewska, M. et al. Subclonal cooperation drives metastasis by modulating local and systemic immune microenvironments. Nat. Cell Biol. 21, 879–888 (2019).
pubmed: 31263265 pmcid: 6609451 doi: 10.1038/s41556-019-0346-x
Juric, D. et al. Convergent loss of PTEN leads to clinical resistance to a PI(3)Kα inhibitor. Nature 518, 240–244 (2015).
pubmed: 25409150 doi: 10.1038/nature13948
Jones, S. et al. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl Acad. Sci. USA 105, 4283–4288 (2008).
pubmed: 18337506 pmcid: 2393770 doi: 10.1073/pnas.0712345105
Shah, S. P. et al. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461, 809–813 (2009).
pubmed: 19812674 doi: 10.1038/nature08489
Casasent, A. K. et al. Multiclonal invasion in breast tumors identified by topographic single cell sequencing. Cell 172, 205–217.e12 (2018).
pubmed: 29307488 pmcid: 5766405 doi: 10.1016/j.cell.2017.12.007
Tarabichi, M. et al. A practical guide to cancer subclonal reconstruction from DNA sequencing. Nat. Methods 18, 144–155 (2021).
pubmed: 33398189 pmcid: 7867630 doi: 10.1038/s41592-020-01013-2
Shen, C. Y. et al. Genome-wide search for loss of heterozygosity using laser capture microdissected tissue of breast carcinoma: an implication for mutator phenotype and breast cancer pathogenesis. Cancer Res. 60, 3884–3892 (2000).
pubmed: 10919664
Zhao, T. et al. Spatial genomics enables multi-modal study of clonal heterogeneity in tissues. Nature 601, 85–91 (2022).
pubmed: 34912115 doi: 10.1038/s41586-021-04217-4
Erickson, A. et al. Spatially resolved clonal copy number alterations in benign and malignant tissue. Nature 608, 360–367 (2022).
pubmed: 35948708 pmcid: 9365699 doi: 10.1038/s41586-022-05023-2
Janiszewska, M. et al. In situ single-cell analysis identifies heterogeneity for PIK3CA mutation and HER2 amplification in HER2-positive breast cancer. Nat. Genet. 47, 1212–1219 (2015).
pubmed: 26301495 pmcid: 4589505 doi: 10.1038/ng.3391
Larsson, C., Grundberg, I., Söderberg, O. & Nilsson, M. In situ detection and genotyping of individual mRNA molecules. Nat. Methods 7, 395–397 (2010).
pubmed: 20383134 doi: 10.1038/nmeth.1448
Grundberg, I. et al. In situ mutation detection and visualization of intratumor heterogeneity for cancer research and diagnostics. Oncotarget 4, 2407–2418 (2013).
pubmed: 24280411 pmcid: 3926836 doi: 10.18632/oncotarget.1527
Ke, R. et al. In situ sequencing for RNA analysis in preserved tissue and cells. Nat. Methods 10, 857–860 (2013).
pubmed: 23852452 doi: 10.1038/nmeth.2563
Baker, A.-M. et al. Robust RNA-based in situ mutation detection delineates colorectal cancer subclonal evolution. Nat. Commun. 8, 1998 (2017).
pubmed: 29222441 pmcid: 5722928 doi: 10.1038/s41467-017-02295-5
Cowell, C. F. et al. Progression from ductal carcinoma in situ to invasive breast cancer: revisited. Mol. Oncol. 7, 859–869 (2013).
pubmed: 23890733 pmcid: 5528459 doi: 10.1016/j.molonc.2013.07.005
Svedlund, J. et al. Generation of in situ sequencing based OncoMaps to spatially resolve gene expression profiles of diagnostic and prognostic markers in breast cancer. EBioMedicine 48, 212–223 (2019).
pubmed: 31526717 pmcid: 6838368 doi: 10.1016/j.ebiom.2019.09.009
Wu, S. Z. et al. A single-cell and spatially resolved atlas of human breast cancers. Nat. Genet. 53, 1334–1347 (2021).
pubmed: 34493872 pmcid: 9044823 doi: 10.1038/s41588-021-00911-1
Ellis, P. et al. Reliable detection of somatic mutations in solid tissues by laser-capture microdissection and low-input DNA sequencing. Nat. Protoc. 16, 841–871 (2021).
pubmed: 33318691 doi: 10.1038/s41596-020-00437-6
Gataric, M. et al. PoSTcode: probabilistic image-based spatial transcriptomics decoder. Preprint at https://doi.org/10.1101/2021.10.12.464086 (2021).
Nirmal, A. J. et al. The spatial landscape of progression and immunoediting in primary melanoma at single-cell resolution. Cancer Discov. 12, 1518–1541 (2022).
pubmed: 35404441 pmcid: 9167783 doi: 10.1158/2159-8290.CD-21-1357
Kole, A. J. et al. Overall survival is improved when DCIS accompanies invasive breast cancer. Sci. Rep. 9, 9934 (2019).
pubmed: 31289308 pmcid: 6616329 doi: 10.1038/s41598-019-46309-2
Going, J. J. & Moffat, D. F. Escaping from flatland: clinical and biological aspects of human mammary duct anatomy in three dimensions. J. Pathol. 203, 538–544 (2004).
pubmed: 15095476 doi: 10.1002/path.1556
Schnitt, S. J. & Collins, L. C. Biopsy Interpretation of the Breast (Lippincott Williams & Wilkins, 2009).
Pinder, S. E. Ductal carcinoma in situ (DCIS): pathological features, differential diagnosis, prognostic factors and specimen evaluation. Mod. Pathol. 23, S8–S13 (2010).
pubmed: 20436505 doi: 10.1038/modpathol.2010.40
Thomson, J. Z. et al. Growth pattern of ductal carcinoma in situ (DCIS): a retrospective analysis based on mammographic findings. Br. J. Cancer 85, 225–227 (2001).
pubmed: 11461081 pmcid: 2364049 doi: 10.1054/bjoc.2001.1877
Solin, L. J. et al. A multigene expression assay to predict local recurrence risk for ductal carcinoma in situ of the breast. J. Natl Cancer Inst. 105, 701–710 (2013).
pubmed: 23641039 pmcid: 3653823 doi: 10.1093/jnci/djt067
Jatoi, I., Hilsenbeck, S. G., Clark, G. M. & Osborne, C. K. Significance of axillary lymph node metastasis in primary breast cancer. J. Clin. Oncol. 17, 2334–2340 (1999)
Sereesongsaeng, N., McDowell, S. H., Burrows, J. F., Scott, C. J. & Burden, R. E. Cathepsin V suppresses GATA3 protein expression in luminal A breast cancer. Breast Cancer Res. 22, 139 (2020).
pubmed: 33298139 pmcid: 7726886 doi: 10.1186/s13058-020-01376-6
Kwon, M. J. et al. CD24 overexpression is associated with poor prognosis in luminal A and triple-negative breast cancer. PLoS ONE 10, e0139112 (2015).
pubmed: 26444008 pmcid: 4596701 doi: 10.1371/journal.pone.0139112
Li, X.-P. et al. Co-expression of CXCL8 and HIF-1α is associated with metastasis and poor prognosis in hepatocellular carcinoma. Oncotarget 6, 22880–22889 (2015).
pubmed: 26078356 pmcid: 4673206 doi: 10.18632/oncotarget.4412
Cairns, R. A. & Hill, R. P. Acute hypoxia enhances spontaneous lymph node metastasis in an orthotopic murine model of human cervical carcinoma. Cancer Res. 64, 2054–2061 (2004).
pubmed: 15026343 doi: 10.1158/0008-5472.CAN-03-3196
Sottoriva, A. et al. A Big Bang model of human colorectal tumor growth. Nat. Genet. 47, 209–216 (2015).
pubmed: 25665006 pmcid: 4575589 doi: 10.1038/ng.3214
Vickovic, S. et al. High-definition spatial transcriptomics for in situ tissue profiling. Nat. Methods 16, 987–990 (2019).
pubmed: 31501547 pmcid: 6765407 doi: 10.1038/s41592-019-0548-y
Gyllborg, D. et al. Hybridization-based in situ sequencing (HybISS) for spatially resolved transcriptomics in human and mouse brain tissue. Nucleic Acids Res. 48, e112 (2020).
pubmed: 32990747 pmcid: 7641728 doi: 10.1093/nar/gkaa792
Lee, H., Marco Salas, S., Gyllborg, D. & Nilsson, M. Direct RNA targeted in situ sequencing for transcriptomic profiling in tissue. Sci. Rep. 12, 7976 (2022).
pubmed: 35562352 pmcid: 9106737 doi: 10.1038/s41598-022-11534-9
Dobzhansky, T. Nothing in biology makes sense except in the light of evolution. Am. Biol. Teach. 35, 125–129 (1973).
doi: 10.2307/4444260

Auteurs

Artem Lomakin (A)

European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Hinxton, UK.
Wellcome Sanger Institute, Hinxton, UK.
Division of AI in Oncology, German Cancer Research Centre DKFZ, Heidelberg, Germany.

Jessica Svedlund (J)

Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, Sweden.

Carina Strell (C)

Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, Sweden.
Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden.

Milana Gataric (M)

European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Hinxton, UK.
Wellcome Sanger Institute, Hinxton, UK.

Artem Shmatko (A)

Division of AI in Oncology, German Cancer Research Centre DKFZ, Heidelberg, Germany.

Gleb Rukhovich (G)

Wellcome Sanger Institute, Hinxton, UK.
Division of AI in Oncology, German Cancer Research Centre DKFZ, Heidelberg, Germany.

Jun Sung Park (JS)

European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Hinxton, UK.
Wellcome Sanger Institute, Hinxton, UK.
Division of AI in Oncology, German Cancer Research Centre DKFZ, Heidelberg, Germany.

Young Seok Ju (YS)

Laboratory of Cancer Genomics, GSMSE, KAIST, Daejeon, Korea.

Stefan Dentro (S)

European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Hinxton, UK.
Wellcome Sanger Institute, Hinxton, UK.
Division of AI in Oncology, German Cancer Research Centre DKFZ, Heidelberg, Germany.

Vitalii Kleshchevnikov (V)

Wellcome Sanger Institute, Hinxton, UK.

Vasyl Vaskivskyi (V)

Wellcome Sanger Institute, Hinxton, UK.

Tong Li (T)

Wellcome Sanger Institute, Hinxton, UK.

Omer Ali Bayraktar (OA)

Wellcome Sanger Institute, Hinxton, UK.

Sarah Pinder (S)

Guys and St Thomas' NHS Trust, London, UK.
School of Cancer & Pharmaceutical Sciences, King's College London, London, UK.

Andrea L Richardson (AL)

Department of Pathology, John Hopkins Medicine, Baltimore, MD, USA.

Sandro Santagata (S)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Laboratory of Systems Pharmacology, Harvard Program in Therapeutic Science, Boston, MA, USA.
Ludwig Center at Harvard, Harvard Medical School, Boston, MA, USA.

Peter J Campbell (PJ)

Wellcome Sanger Institute, Hinxton, UK.

Hege Russnes (H)

Department of Pathology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.
Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Moritz Gerstung (M)

European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Hinxton, UK. moritz.gerstung@dkfz.de.
Division of AI in Oncology, German Cancer Research Centre DKFZ, Heidelberg, Germany. moritz.gerstung@dkfz.de.

Mats Nilsson (M)

Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, Sweden. mats.nilsson@scilifelab.se.

Lucy R Yates (LR)

Wellcome Sanger Institute, Hinxton, UK. ly2@sanger.ac.uk.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH