https://doi.org/10.1038/s41586-023-05729-x · 
Видання: Nature, 2023, №7957, с.534-542
Видавець: Springer Science and Business Media LLC
Автори:
- Maise Al Bakir
- Ariana Huebner
- Carlos Martínez-Ruiz
- Kristiana Grigoriadis
- Thomas B. K. Watkins
- Oriol Pich
- David A. Moore
- Selvaraju Veeriah
- Sophia Ward
- Joanne Layco*ck
- Diana Johnson
- Andrew Rowan
- Maryam Razaq
- Mita Akther
- Cristina Naceur-Lombardelli
- Paulina Prymas
- Antonia Toncheva
- Sonya Hessey
- Michelle Dietzen
- Emma Colliver
- Alexander M. Frankell
- Abigail Bunkum
- Emilia L. Lim
- Takahiro Karasaki
- Christopher Abbosh
- Crispin T. Hiley
- Mark S. Hill
- Daniel E. Cook
- Gareth A. Wilson
- Roberto Salgado
- Emma Nye
- Richard Kevin Stone
- Dean A. Fennell
- Gillian Price
- Keith M. Kerr
- Babu Naidu
- Gary Middleton
- Yvonne Summers
- Colin R. Lindsay
- Fiona H. Blackhall
- Judith Cave
- Kevin G. Blyth
- Arjun Nair
- Asia Ahmed
- Magali N. Taylor
- Alexander James Procter
- Mary Falzon
- David Lawrence
- Neal Navani
- Ricky M. Thakrar
- Sam M. Janes
- Dionysis Papadatos-Pastos
- Martin D. Forster
- Siow Ming Lee
- Tanya Ahmad
- Sergio A. Quezada
- Karl S. Peggs
- Peter Van Loo
- Caroline Dive
- Allan Hackshaw
- Nicolai J. Birkbak
- Simone Zaccaria
- Jason F. Lester
- Amrita Bajaj
- Apostolos Nakas
- Azmina Sodha-Ramdeen
- Keng Ang
- Mohamad Tufail
- Mohammed Fiyaz Chowdhry
- Molly Scotland
- Rebecca Boyles
- Sridhar Rathinam
- Claire Wilson
- Domenic Marrone
- Sean Dulloo
- Gurdeep Matharu
- Jacqui A. Shaw
- Joan Riley
- Lindsay Primrose
- Ekaterini Boleti
- Heather Cheyne
- Mohammed Khalil
- Shirley Richardson
- Tracey Cruickshank
- Sarah Benafif
- Kayleigh Gilbert
- Akshay J. Patel
- Aya Osman
- Christer Lacson
- Gerald Langman
- Helen Shackleford
- Madava Djearaman
- Salma Kadiri
- Angela Leek
- Jack Davies Hodgkinson
- Nicola Totten
- Angeles Montero
- Elaine Smith
- Eustace Fontaine
- Felice Granato
- Helen Doran
- Juliette Novasio
- Kendadai Rammohan
- Leena Joseph
- Paul Bishop
- Rajesh Shah
- Stuart Moss
- Vijay Joshi
- Philip Crosbie
- Fabio Gomes
- Kate Brown
- Mathew Carter
- Anshuman Chaturvedi
- Lynsey Priest
- Pedro Oliveira
- Matthew G. Krebs
- Alexandra Clipson
- Jonathan Tugwood
- Alastair Kerr
- Dominic G. Rothwell
- Elaine Kilgour
- Hugo J. W. L. Aerts
- Roland F. Schwarz
- Tom L. Kaufmann
- Rachel Rosenthal
- Zoltan Szallasi
- Judit Kisistok
- Mateo Sokac
- Miklos Diossy
- Jonas Demeulemeester
- Aengus Stewart
- Alastair Magness
- Angeliki Karamani
- Benny Chain
- Brittany B. Campbell
- Carla Castignani
- Chris Bailey
- Clare Puttick
- Clare E. Weeden
- Claudia Lee
- Corentin Richard
- David R. Pearce
- Despoina Karagianni
- Dhruva Biswas
- Dina Levi
- Elena Hoxha
- Elizabeth Larose Cadieux
- Eva Grönroos
- Felip Gálvez-Cancino
- Foteini Athanasopoulou
- Francisco Gimeno-Valiente
- George Kassiotis
- Georgia Stavrou
- Gerasimos Mastrokalos
- Haoran Zhai
- Helen L. Lowe
- Ignacio Matos
- Jacki Goldman
- James L. Reading
- James R. M. Black
- Javier Herrero
- Jayant K. Rane
- Jerome Nicod
- Jie Min Lam
- John A. Hartley
- Katey S. S. Enfield
- Kayalvizhi Selvaraju
- Kerstin Thol
- Kevin Litchfield
- Kevin W. Ng
- Kezhong Chen
- Krijn Dijkstra
- Krupa Thakkar
- Leah Ensell
- Mansi Shah
- Marcos Vasquez
- Maria Litovchenko
- Mariana Werner Sunderland
- Michelle Leung
- Mickael Escudero
- Mihaela Angelova
- Miljana Tanić
- Monica Sivakumar
- Nnennaya Kanu
- Olga Chervova
- Olivia Lucas
- Othman Al-Sawaf
- Philip Hobson
- Piotr Pawlik
- Robert Bentham
- Robert E. Hynds
- Roberto Vendramin
- Sadegh Saghafinia
- Saioa López
- Samuel Gamble
- Seng Kuong Anakin Ung
- Sharon Vanloo
- Stefan Boeing
- Stephan Beck
- Supreet Kaur Bola
- Tamara Denner
- Teresa Marafioti
- Thanos P. Mourikis
- Victoria Spanswick
- Vittorio Barbè
- Wei-Ting Lu
- William Hill
- Wing Kin Liu
- Yin Wu
- Yutaka Naito
- Zoe Ramsden
- Catarina Veiga
- Gary Royle
- Charles-Antoine Collins-Fekete
- Francesco Fraioli
- Paul Ashford
- Tristan Clark
- Elaine Borg
- James Wilson
- Davide Patrini
- Emilie Martinoni Hoogenboom
- Fleur Monk
- James W. Holding
- Junaid Choudhary
- Kunal Bhakhri
- Marco Scarci
- Martin Hayward
- Nikolaos Panagiotopoulos
- Pat Gorman
- Reena Khiroya
- Robert C. M. Stephens
- Yien Ning Sophia Wong
- Steve Bandula
- Abigail Sharp
- Sean Smith
- Nicole Gower
- Harjot Kaur Dhanda
- Kitty Chan
- Camilla Pilotti
- Rachel Leslie
- Anca Grapa
- Hanyun Zhang
- Khalid AbdulJabbar
- Xiaoxi Pan
- Yinyin Yuan
- David Chuter
- Mairead MacKenzie
- Serena Chee
- Aiman Alzetani
- Lydia Scarlett
- Jennifer Richards
- Papawadee Ingram
- Silvia Austin
- Eric Lim
- Paulo De Sousa
- Simon Jordan
- Alexandra Rice
- Hilgardt Raubenheimer
- Harshil Bhayani
- Lyn Ambrose
- Anand Devaraj
- Hema Chavan
- Sofina Begum
- Silviu I. Buderi
- Daniel Kaniu
- Mpho Malima
- Sarah Booth
- Andrew G. Nicholson
- Nadia Fernandes
- Pratibha Shah
- Chiara Proli
- Madeleine Hewish
- Sarah Danson
- Michael J. Shackcloth
- Lily Robinson
- Peter Russell
- Craig Dick
- John Le Quesne
- Alan Kirk
- Mo Asif
- Rocco Bilancia
- Nikos Kostoulas
- Mathew Thomas
- Mariam Jamal-Hanjani
- Nicholas McGranahan
- Charles Swanton
- TRACERx Consortium
Анотація
AbstractMetastatic disease is responsible for the majority of cancer-related deaths1. We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasis-seeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site of recurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse.
Список літератури
- Bray, F. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68, 394–424 (2018).
https://doi.org/10.3322/caac.21492 - Zappa, C. & Mousa, S. A. Non-small cell lung cancer: current treatment and future advances. Transl. Lung Cancer Res. 5, 288–300 (2016).
https://doi.org/10.21037/tlcr.2016.06.07 - Jamal-Hanjani, M. et al. Tracking the evolution of non–small-cell lung cancer. N. Engl. J. Med. 376, 2109–2121 (2017).
https://doi.org/10.1056/NEJMoa1616288 - Grigoriadis, K. et al. CONIPHER: a computational framework for scalable phylogenetic reconstruction with error correction. Protoc. Exchange https://doi.org/10.21203/rs.3.pex-2158/v1 (2023).
https://doi.org/10.21203/rs.3.pex-2158/v1 - de Bruin, E. C. et al. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 346, 251–256 (2014).
https://doi.org/10.1126/science.1253462 - Pich, O. et al. The mutational footprints of cancer therapies. Nat. Genet. 51, 1732–1740 (2019).
https://doi.org/10.1038/s41588-019-0525-5 - Landau, H. J. et al. Accelerated single cell seeding in relapsed multiple myeloma. Nat. Commun. 11, 3617 (2020).
https://doi.org/10.1038/s41467-020-17459-z - Pich, O. et al. The evolution of hematopoietic cells under cancer therapy. Nat. Commun. 12, 4803 (2021).
https://doi.org/10.1038/s41467-021-24858-3 - Sun, R. et al. Between-region genetic divergence reflects the mode and tempo of tumor evolution. Nat. Genet. 49, 1015–1024 (2017).
https://doi.org/10.1038/ng.3891 - Bueno, J., Landeras, L. & Chung, J. H. Updated Fleischner society guidelines for managing incidental pulmonary nodules: common questions and challenging scenarios. Radiographics 38, 1337–1350 (2018).
https://doi.org/10.1148/rg.2018180017 - Callister, M. E. J. et al. British Thoracic Society guidelines for the investigation and management of pulmonary nodules. Thorax 70, ii1–ii54 (2015).
https://doi.org/10.1136/thoraxjnl-2015-207168 - Horeweg, N. et al. Lung cancer probability in patients with CT-detected pulmonary nodules: a prespecified analysis of data from the NELSON trial of low-dose CT screening. Lancet Oncol. 15, 1332–1341 (2014).
https://doi.org/10.1016/S1470-2045(14)70389-4 - de Koning, H. J. et al. Reduced lung-cancer mortality with volume CT screening in a randomized trial. N. Engl. J. Med. 382, 503–513 (2020).
https://doi.org/10.1056/NEJMoa1911793 - Oudkerk, M. et al. European position statement on lung cancer screening. Lancet Oncol. 18, e754–e766 (2017).
https://doi.org/10.1016/S1470-2045(17)30861-6 - MacMahon, H. et al. Guidelines for management of incidental pulmonary nodules detected on CT images: from the Fleischner Society 2017. Radiology 284, 228–243 (2017).
https://doi.org/10.1148/radiol.2017161659 - American College of Radiology Committee on Lung-RADS. Lung-RADS Assessment Categories version 1.1 (ACR, 2019); https://www.acr.org/-/media/ACR/Files/RADS/Lung-RADS/LungRADSAssessmentCategoriesv1-1.pdf.
- Frankell, A. M. et al. The evolution of lung cancer and impact of subclonal selection in TRACERx. Nature https://doi.org/10.1038/s41586-023-05783-5 (2023).
https://doi.org/10.1038/s41586-023-05783-5 - El-Kebir, M., Satas, G. & Raphael, B. J. Inferring parsimonious migration histories for metastatic cancers. Nat. Genet. 50, 718–726 (2018).
https://doi.org/10.1038/s41588-018-0106-z - Abbosh, C. et al. Tracking early lung cancer metastatic dissemination in TRACERx using ctDNA. Nature https://doi.org/10.1038/s41586-023-05776-4 (2023).
https://doi.org/10.1038/s41586-023-05776-4 - Martincorena, I. et al. Universal patterns of selection in cancer and somatic tissues. Cell 171, 1029–1041 (2017).
https://doi.org/10.1016/j.cell.2017.09.042 - Bailey, M. H. et al. Comprehensive characterization of cancer driver genes and mutations. Cell 174, 1034–1035 (2018).
https://doi.org/10.1016/j.cell.2018.07.034 - Mermel, C. H. et al. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol. 12, R41 (2011).
https://doi.org/10.1186/gb-2011-12-4-r41 - Lee, W.-C. et al. Multiomics profiling of primary lung cancers and distant metastases reveals immunosuppression as a common characteristic of tumor cells with metastatic plasticity. Genome Biol. 21, 271 (2020).
https://doi.org/10.1186/s13059-020-02175-0 - Brown, D. et al. Phylogenetic analysis of metastatic progression in breast cancer using somatic mutations and copy number aberrations. Nat. Commun. 8, 14944 (2017).
https://doi.org/10.1038/ncomms14944 - Faltas, B. M. et al. Clonal evolution of chemotherapy-resistant urothelial carcinoma. Nat. Genet. 48, 1490–1499 (2016).
https://doi.org/10.1038/ng.3692 - Hu, Z. et al. Quantitative evidence for early metastatic seeding in colorectal cancer. Nat. Genet. 51, 1113–1122 (2019).
https://doi.org/10.1038/s41588-019-0423-x - Naxerova, K. et al. Origins of lymphatic and distant metastases in human colorectal cancer. Science 357, 55–60 (2017).
https://doi.org/10.1126/science.aai8515 - Kim, T.-M. et al. Subclonal genomic architectures of primary and metastatic colorectal cancer based on intratumoral genetic heterogeneity. Clin. Cancer Res. 21, 4461–4472 (2015).
https://doi.org/10.1158/1078-0432.CCR-14-2413 - Zhao, Z.-M. et al. Early and multiple origins of metastatic lineages within primary tumors. Proc. Natl Acad. Sci. USA 113, 2140–2145 (2016).
https://doi.org/10.1073/pnas.1525677113 - Zhai, W. et al. The spatial organization of intra-tumour heterogeneity and evolutionary trajectories of metastases in hepatocellular carcinoma. Nat. Commun. 8, 4565 (2017).
https://doi.org/10.1038/ncomms14565 - Gibson, W. J. et al. The genomic landscape and evolution of endometrial carcinoma progression and abdominopelvic metastasis. Nat. Genet. 48, 848–855 (2016).
https://doi.org/10.1038/ng.3602 - Reiter, J. G. et al. Lymph node metastases develop through a wider evolutionary bottleneck than distant metastases. Nat. Genet. 52, 692–700 (2020).
https://doi.org/10.1038/s41588-020-0633-2 - Tang, W.-F. et al. Timing and origins of local and distant metastases in lung cancer. J. Thorac. Oncol. 16, 1136–1148 (2021).
https://doi.org/10.1016/j.jtho.2021.02.023 - Tan, Q. et al. Genomic alteration during metastasis of lung adenocarcinoma. Cell. Physiol. Biochem. 38, 469–486 (2016).
https://doi.org/10.1159/000438644 - Hu, Z., Li, Z., Ma, Z. & Curtis, C. Multi-cancer analysis of clonality and the timing of systemic spread in paired primary tumors and metastases. Nat. Genet. 52, 701–708 (2020).
https://doi.org/10.1038/s41588-020-0628-z - Ullah, I. et al. Evolutionary history of metastatic breast cancer reveals minimal seeding from axillary lymph nodes. J. Clin. Invest. 128, 1355–1370 (2018).
https://doi.org/10.1172/JCI96149 - Haffner, M. C. et al. Tracking the clonal origin of lethal prostate cancer. J. Clin. Invest. 123, 4918–4922 (2013).
https://doi.org/10.1172/JCI70354 - Noorani, A. et al. Genomic evidence supports a clonal diaspora model for metastases of esophageal adenocarcinoma. Nat. Genet. 52, 74–83 (2020).
https://doi.org/10.1038/s41588-019-0551-3 - Gundem, G. et al. The evolutionary history of lethal metastatic prostate cancer. Nature 520, 353–357 (2015).
https://doi.org/10.1038/nature14347 - Chen, H.-N. et al. Genomic evolution and diverse models of systemic metastases in colorectal cancer. Gut 71, 322–332 (2022).
https://doi.org/10.1136/gutjnl-2020-323703 - Abbosh, C. et al. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature 545, 446–451 (2017).
https://doi.org/10.1038/nature22364 - Turajlic, S. et al. Tracking cancer evolution reveals constrained routes to metastases: TRACERx renal. Cell 173, 581–594 (2018).
https://doi.org/10.1016/j.cell.2018.03.057 - Bailey, C. et al. Tracking cancer evolution through the disease course. Cancer Discov. 11, 916–932 (2021).
https://doi.org/10.1158/2159-8290.CD-20-1559 - Rosenthal, R., McGranahan, N., Herrero, J., Taylor, B. S. & Swanton, C. DeconstructSigs: delineating mutational processes in single tumors distinguishes DNA repair deficiencies and patterns of carcinoma evolution. Genome Biol. 17, 31 (2016).
https://doi.org/10.1186/s13059-016-0893-4 - Alexandrov, L. B. et al. The repertoire of mutational signatures in human cancer. Nature 578, 94–101 (2020).
https://doi.org/10.1038/s41586-020-1943-3 - Boot, A. et al. In-depth characterization of the cisplatin mutational signature in human cell lines and in esophageal and liver tumors. Genome Res. 28, 654–665 (2018).
https://doi.org/10.1101/gr.230219.117 - Sottoriva, A. et al. A Big Bang model of human colorectal tumor growth. Nat. Genet. 47, 209–216 (2015).
https://doi.org/10.1038/ng.3214 - Cannataro, V. L., McKinley, S. A. & St Mary, C. M. The implications of small stem cell niche sizes and the distribution of fitness effects of new mutations in aging and tumorigenesis. Evol. Appl. 9, 565–582 (2016).
https://doi.org/10.1111/eva.12361 - Lebeuf-Taylor, E., McCloskey, N., Bailey, S. F., Hinz, A. & Kassen, R. The distribution of fitness effects among synonymous mutations in a gene under directional selection. eLife 8, e45952 (2019).
https://doi.org/10.7554/eLife.45952 - Eyre-Walker, A. & Keightley, P. D. The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8, 610–618 (2007).
https://doi.org/10.1038/nrg2146 - Bozic, I. et al. Accumulation of driver and passenger mutations during tumor progression. Proc. Natl Acad. Sci. USA 107, 18545–18550 (2010).
https://doi.org/10.1073/pnas.1010978107 - Williams, M. J. et al. Measuring the distribution of fitness effects in somatic evolution by combining clonal dynamics with dN/dS ratios. eLife 9, e48714 (2020).
https://doi.org/10.7554/eLife.48714 - Turajlic, S., Sottoriva, A., Graham, T. & Swanton, C. Resolving genetic heterogeneity in cancer. Nat. Rev. Genet. 20, 404–416 (2019).
https://doi.org/10.1038/s41576-019-0114-6 - Venkatesan, S. et al. Induction of APOBEC3 exacerbates DNA replication stress and chromosomal instability in early breast and lung cancer evolution. Cancer Discov. 11, 2456–2473 (2021).
https://doi.org/10.1158/2159-8290.CD-20-0725 - Dewhurst, S. M. et al. Tolerance of whole-genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discov. 4, 175–185 (2014).
https://doi.org/10.1158/2159-8290.CD-13-0285 - Werner, B. et al. Measuring single cell divisions in human tissues from multi-region sequencing data. Nat. Commun. 11, 1035 (2020).
https://doi.org/10.1038/s41467-020-14844-6 - Del Monte, U. Does the cell number 109 still really fit one gram of tumor tissue? Cell Cycle 8, 505–506 (2009).
https://doi.org/10.4161/cc.8.3.7608 - McGranahan, N. et al. Clonal status of actionable driver events and the timing of mutational processes in cancer evolution. Sci. Transl. Med. 7, 283ra54 (2015).
https://doi.org/10.1126/scitranslmed.aaa1408 - Berger, A. H. et al. High-throughput phenotyping of lung cancer somatic mutations. Cancer Cell 30, 214 (2016).
https://doi.org/10.1016/j.ccell.2016.06.022 - Lawson, A. R. J. et al. Extensive heterogeneity in somatic mutation and selection in the human bladder. Science 370, 75–82 (2020).
https://doi.org/10.1126/science.aba8347 - Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289–300 (1995).
- Watkins, T. B. K. et al. Pervasive chromosomal instability and karyotype order in tumour evolution. Nature 587, 126–132 (2020).
https://doi.org/10.1038/s41586-020-2698-6 - Frankell A. M., Colliver E., Mcgranahan N., Swanton C. cloneMap: a R package to visualise clonal heterogeneity. Preprint at bioRxiv https://doi.org/10.1101/2022.07.26.501523 (2022).
https://doi.org/10.1101/2022.07.26.501523
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