Somatic evolution following cancer treatment in normal tissue

Oriol Pich^{1

2}, Sophia Ward^{3

4

5}, Andrew Rowan³, Cristina Naceur-Lombardelli^{4

6}, Oliver Shutkever^{4

6

7}, Carlos Martinez-Ruiz^{4

8}, Siân Harries^{3

4

5}, Sonya Hessey^{4

6

9}, Babu Naidu¹⁰, James D Brenton^{11

12

13}, John Le Quesne^{14

15

16}, Anne Thomas¹⁷, Cathy Richards¹⁸, Matthew G Krebs^{19

20

21}, Samra Turajlic^{20

22

23

24

25}, Sanjay Jogai^{26

27}, Simone Zaccaria^{4

9}, David Moore^{3

4

28}, Crispin T Hiley^{7

29}; PEACE Consortium; Charles Swanton^{30

31

32}, Mariam Jamal-Hanjani^{33

34

35}, Nicholas McGranahan^{36

37}

Collaborators, Affiliations

Collaborators

PEACE Consortium:
John Le Quesne, Kai-Keen Shiu, John Bridgewater, Daniel Hochhauser, Martin Forster, Siow Ming Lee, Tanya Ahmad, Dionysis Papadatos-Pastos, Sam Janes, Peter Van Loo, Katey Enfield, Ariana Huebner, Sergio Quezada, Stephan Beck, Tariq Enver, David R Pearce, Mary Falzon, Ron Sinclair, Zoe Rhodes, Teresa Marafioti, Miriam Mitchison, Mark Linch, Sebastian Brandner, Selvaraju Veeriah, Heather Shaw, Gerhardt Attard, Faye Gishen, Maise Al-Bakir, Nnenna Kanu, Francisco Gimeno-Valiente, Emilia L Lim, James Reading, Benny Chain, Adrienne Flanagan, Emma Colliver, Mihaela Angelova, James Black, Olivia Lucas, William Hill, Wing Kin Liu, Alexander Frankell, Roberto Salgado, Kristiana Grigoriadis, Takahiro Karasaki, Abigail Bunkum, Sarah Benafif, Vittorio Barbè, Supreet Kaur Bola, Osvaldas Vainauskas, Anna Wingate, Daniel Wetterskog, A M Mahedi Hasan, Stefano Lise, Gianmarco Leone, Anuradha Jayaram, Constantine Alifrangis, Ursula McGovern, Kerstin Thol, Samuel Gamble, Seng Kuong Ung, Piotr Pawlik, Roberto Vendramin, Jayant Rane, Angela Dwornik, Kerry Bowles, Jeanette Kittel, Kerstin Haase, Rija Zaidi, Athanasia Vargiamiou, Lucrezia Patruno, Christopher Aled Chamberlain, Welles Robinson, Iain McNeish, Nataly Ojeda Mosquera, Jiali Liu, Felix O'Farrell, Chenelle Marcel, James Larkin, Lisa Pickering, Andrew Furness, Kate Young, Will Drake, Kim Edmonds, Nikki Hunter, Mary Mangwende, Lauren Grostate, Lavinia Spain, Scott Shepherd, Haixi Yan, Benjamin Shum, Zayd Tippu, Brian Hanley, Charlotte Spencer, Max Emmerich, Camille Gerard, Eleanor Carlyle, Steve Hazell, Hardeep Mudhar, Christina Messiou, Arash Latifoltojar, Annika Fendler, Fiona Byrne, Husayn Pallikonda, Irene Lobon, Alexander Coulton, Anne-Laure Cattin, Daqi Deng, Hugang Feng, Nadia Yousaf, Sanjay Popat, Charlotte Milner-Watts, Emma Nye, Aida Murra, Justine Korteweg, Lauren Terry, Jennifer Biano, Kema Peat, Emma Turay, Peter Hill, Marija Miletic, Anadil Javaid, Jennifer Thomas, Bakir Kudic, Orla McGowan, Dharmista Ramesh, Oznur Saka, Sinem Arslan, Laura Marandino, Reina Ammar, Gurneet Kapur, Dilruba Kabir, David McMahon, Alexius John, Foteini Kalofonou, Debra Josephs, Sheeba Irshad, James Spicer, Anna Green, Ruby Stewart, Natasha Wright, Ruxandra Mitu, Deborah Enting, Sarah Rudman, Sharmistha Ghosh, Eleni Karapanagiotou, Elias Pintus, Andrew Tutt, Nicola Thompson, Rebecca Fitzgerald, Merche Jimenez-Linan, Elena Provenzano, Anna Paterson, Kieren Allinson, Grant D Stewart, Ultan McDermott, Tim Maughan, Olaf Ansorge, Peter Campbell, Patricia Roxburgh, Sioban Fraser, Kevin Blyth, Fiona Blackhall, Yvonne Summers, Pedro Oliveira, Caroline Dive, Fabio Gomes, Mat Carter, Dean Fennell, Jacqui Shaw, Claire Wilson, Charlotte Poile, Kudazyi H Kutywayo, Maurice R Dungey, Jens Claus Hahne, Shobhit Baijal, Gerald Langman, Charlotte Ferris, Hollie Bancroft, Amy Kerr, Gary Middleton, Joanne Webb, Salma Kadiri, Bernard Olisemeke, Rodelaine Wilson, Aya Osman, Ian Tomlinson, Judith Cave, Luke Nolan, Samantha Holden, Tania Fernandes, Dave Chuter, Mairead McKenzie, Allan Hackshaw, Aoife Walker, Hayley Bridger, Rachel Leslie, Shivani Patel

Affiliations

¹ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, UK. oriol.pich@crick.ac.uk.
² Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. oriol.pich@crick.ac.uk.
³ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, UK.
⁴ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK.
⁵ Genomics Science Technology Platform, The Francis Crick Institute, London, UK.
⁶ Cancer Metastasis Laboratory, University College London Cancer Institute, London, UK.
⁷ University College London Hospitals, London, UK.
⁸ Cancer Genome Evolution Research Group, University College London Cancer Institute, London, UK.
⁹ Computational Cancer Genomics Research Group, University College London Cancer Institute, London, UK.
¹⁰ Birmingham Acute Care Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK.
¹¹ Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Cambridge, UK.
¹² Cancer Research UK Major Centre-Cambridge, University of Cambridge, Cambridge, UK.
¹³ Cambridge University Hospital NHS Foundation Trust and National Institute for Health Research Cambridge Biomedical Research Centre, Addenbrooke's Hospital, Cambridge, UK.
¹⁴ Cancer Research UK Scotland Institute, Glasgow, UK.
¹⁵ School of Cancer Sciences, University of Glasgow, Glasgow, UK.
¹⁶ NHS Greater Glasgow and Clyde Pathology Department, Queen Elizabeth University Hospital, Glasgow, UK.
¹⁷ Leicester Cancer Research Centre, College of Life Sciences, University of Leicester, Leicester, UK.
¹⁸ University Hospitals of Leicester NHS Trust, Leicester, UK.
¹⁹ Division of Cancer Sciences, The University of Manchester, Manchester, UK.
²⁰ The Christie NHS Foundation Trust, Manchester, UK.
²¹ National Institute for Health and Care Research (NIHR) Manchester Biomedical Research Centre (BRC), Manchester, UK.
²² The Royal Marsden Hospital, London, UK.
²³ The Institute of Cancer Research, London, UK.
²⁴ Cancer Dynamics Laboratory, The Francis Crick Institute, London, UK.
²⁵ Cancer Dynamics Laboratory, The CRUK Manchester Institute, Manchester, UK.
²⁶ NIHR Biomedical Research Centre, School of Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
²⁷ University Hospital Southampton NHS Trust, Southampton, UK.
²⁸ Department of Cellular Pathology, University College London Hospitals, London, UK.
²⁹ University College London Cancer Institute, London, UK.
³⁰ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, UK. charles.swanton@crick.ac.uk.
³¹ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. charles.swanton@crick.ac.uk.
³² University College London Hospitals, London, UK. charles.swanton@crick.ac.uk.
³³ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. m.jamal-hanjani@ucl.ac.uk.
³⁴ Cancer Metastasis Laboratory, University College London Cancer Institute, London, UK. m.jamal-hanjani@ucl.ac.uk.
³⁵ University College London Hospitals, London, UK. m.jamal-hanjani@ucl.ac.uk.
³⁶ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. nicholas.mcgranahan.10@ucl.ac.uk.
³⁷ Cancer Genome Evolution Research Group, University College London Cancer Institute, London, UK. nicholas.mcgranahan.10@ucl.ac.uk.

PMID: 41372419
DOI: 10.1038/s41586-025-09792-4

Somatic evolution following cancer treatment in normal tissue

Oriol Pich et al. Nature. 2025.

. 2025 Dec 10.

doi: 10.1038/s41586-025-09792-4. Online ahead of print.

Authors

Collaborators

PEACE Consortium:
John Le Quesne, Kai-Keen Shiu, John Bridgewater, Daniel Hochhauser, Martin Forster, Siow Ming Lee, Tanya Ahmad, Dionysis Papadatos-Pastos, Sam Janes, Peter Van Loo, Katey Enfield, Ariana Huebner, Sergio Quezada, Stephan Beck, Tariq Enver, David R Pearce, Mary Falzon, Ron Sinclair, Zoe Rhodes, Teresa Marafioti, Miriam Mitchison, Mark Linch, Sebastian Brandner, Selvaraju Veeriah, Heather Shaw, Gerhardt Attard, Faye Gishen, Maise Al-Bakir, Nnenna Kanu, Francisco Gimeno-Valiente, Emilia L Lim, James Reading, Benny Chain, Adrienne Flanagan, Emma Colliver, Mihaela Angelova, James Black, Olivia Lucas, William Hill, Wing Kin Liu, Alexander Frankell, Roberto Salgado, Kristiana Grigoriadis, Takahiro Karasaki, Abigail Bunkum, Sarah Benafif, Vittorio Barbè, Supreet Kaur Bola, Osvaldas Vainauskas, Anna Wingate, Daniel Wetterskog, A M Mahedi Hasan, Stefano Lise, Gianmarco Leone, Anuradha Jayaram, Constantine Alifrangis, Ursula McGovern, Kerstin Thol, Samuel Gamble, Seng Kuong Ung, Piotr Pawlik, Roberto Vendramin, Jayant Rane, Angela Dwornik, Kerry Bowles, Jeanette Kittel, Kerstin Haase, Rija Zaidi, Athanasia Vargiamiou, Lucrezia Patruno, Christopher Aled Chamberlain, Welles Robinson, Iain McNeish, Nataly Ojeda Mosquera, Jiali Liu, Felix O'Farrell, Chenelle Marcel, James Larkin, Lisa Pickering, Andrew Furness, Kate Young, Will Drake, Kim Edmonds, Nikki Hunter, Mary Mangwende, Lauren Grostate, Lavinia Spain, Scott Shepherd, Haixi Yan, Benjamin Shum, Zayd Tippu, Brian Hanley, Charlotte Spencer, Max Emmerich, Camille Gerard, Eleanor Carlyle, Steve Hazell, Hardeep Mudhar, Christina Messiou, Arash Latifoltojar, Annika Fendler, Fiona Byrne, Husayn Pallikonda, Irene Lobon, Alexander Coulton, Anne-Laure Cattin, Daqi Deng, Hugang Feng, Nadia Yousaf, Sanjay Popat, Charlotte Milner-Watts, Emma Nye, Aida Murra, Justine Korteweg, Lauren Terry, Jennifer Biano, Kema Peat, Emma Turay, Peter Hill, Marija Miletic, Anadil Javaid, Jennifer Thomas, Bakir Kudic, Orla McGowan, Dharmista Ramesh, Oznur Saka, Sinem Arslan, Laura Marandino, Reina Ammar, Gurneet Kapur, Dilruba Kabir, David McMahon, Alexius John, Foteini Kalofonou, Debra Josephs, Sheeba Irshad, James Spicer, Anna Green, Ruby Stewart, Natasha Wright, Ruxandra Mitu, Deborah Enting, Sarah Rudman, Sharmistha Ghosh, Eleni Karapanagiotou, Elias Pintus, Andrew Tutt, Nicola Thompson, Rebecca Fitzgerald, Merche Jimenez-Linan, Elena Provenzano, Anna Paterson, Kieren Allinson, Grant D Stewart, Ultan McDermott, Tim Maughan, Olaf Ansorge, Peter Campbell, Patricia Roxburgh, Sioban Fraser, Kevin Blyth, Fiona Blackhall, Yvonne Summers, Pedro Oliveira, Caroline Dive, Fabio Gomes, Mat Carter, Dean Fennell, Jacqui Shaw, Claire Wilson, Charlotte Poile, Kudazyi H Kutywayo, Maurice R Dungey, Jens Claus Hahne, Shobhit Baijal, Gerald Langman, Charlotte Ferris, Hollie Bancroft, Amy Kerr, Gary Middleton, Joanne Webb, Salma Kadiri, Bernard Olisemeke, Rodelaine Wilson, Aya Osman, Ian Tomlinson, Judith Cave, Luke Nolan, Samantha Holden, Tania Fernandes, Dave Chuter, Mairead McKenzie, Allan Hackshaw, Aoife Walker, Hayley Bridger, Rachel Leslie, Shivani Patel

Affiliations

¹ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, UK. oriol.pich@crick.ac.uk.
² Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. oriol.pich@crick.ac.uk.
³ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, UK.
⁴ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK.
⁵ Genomics Science Technology Platform, The Francis Crick Institute, London, UK.
⁶ Cancer Metastasis Laboratory, University College London Cancer Institute, London, UK.
⁷ University College London Hospitals, London, UK.
⁸ Cancer Genome Evolution Research Group, University College London Cancer Institute, London, UK.
⁹ Computational Cancer Genomics Research Group, University College London Cancer Institute, London, UK.
¹⁰ Birmingham Acute Care Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK.
¹¹ Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Cambridge, UK.
¹² Cancer Research UK Major Centre-Cambridge, University of Cambridge, Cambridge, UK.
¹³ Cambridge University Hospital NHS Foundation Trust and National Institute for Health Research Cambridge Biomedical Research Centre, Addenbrooke's Hospital, Cambridge, UK.
¹⁴ Cancer Research UK Scotland Institute, Glasgow, UK.
¹⁵ School of Cancer Sciences, University of Glasgow, Glasgow, UK.
¹⁶ NHS Greater Glasgow and Clyde Pathology Department, Queen Elizabeth University Hospital, Glasgow, UK.
¹⁷ Leicester Cancer Research Centre, College of Life Sciences, University of Leicester, Leicester, UK.
¹⁸ University Hospitals of Leicester NHS Trust, Leicester, UK.
¹⁹ Division of Cancer Sciences, The University of Manchester, Manchester, UK.
²⁰ The Christie NHS Foundation Trust, Manchester, UK.
²¹ National Institute for Health and Care Research (NIHR) Manchester Biomedical Research Centre (BRC), Manchester, UK.
²² The Royal Marsden Hospital, London, UK.
²³ The Institute of Cancer Research, London, UK.
²⁴ Cancer Dynamics Laboratory, The Francis Crick Institute, London, UK.
²⁵ Cancer Dynamics Laboratory, The CRUK Manchester Institute, Manchester, UK.
²⁶ NIHR Biomedical Research Centre, School of Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
²⁷ University Hospital Southampton NHS Trust, Southampton, UK.
²⁸ Department of Cellular Pathology, University College London Hospitals, London, UK.
²⁹ University College London Cancer Institute, London, UK.
³⁰ Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, London, UK. charles.swanton@crick.ac.uk.
³¹ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. charles.swanton@crick.ac.uk.
³² University College London Hospitals, London, UK. charles.swanton@crick.ac.uk.
³³ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. m.jamal-hanjani@ucl.ac.uk.
³⁴ Cancer Metastasis Laboratory, University College London Cancer Institute, London, UK. m.jamal-hanjani@ucl.ac.uk.
³⁵ University College London Hospitals, London, UK. m.jamal-hanjani@ucl.ac.uk.
³⁶ Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK. nicholas.mcgranahan.10@ucl.ac.uk.
³⁷ Cancer Genome Evolution Research Group, University College London Cancer Institute, London, UK. nicholas.mcgranahan.10@ucl.ac.uk.

PMID: 41372419
DOI: 10.1038/s41586-025-09792-4

Abstract

The extent to which exogenous sources, including cancer treatment, contribute to somatic evolution in normal tissue remains unclear. Here we used high-depth duplex sequencing¹ (more than 30,000× coverage) to analyse 168 cancer-free samples representing 16 organs from 22 patients with metastatic cancer enroled in the PEACE research autopsy study. In every sample, we identified somatic mutations (range 305-2,854 mutations) at low variant allele frequencies (median 0.0000323). We extracted 16 distinct single-base substitution mutational signatures, reflecting processes that have moulded the genomes of normal cells. We identified alcohol-induced mutation acquisition in liver, smoking-induced mutagenesis in lung and cardiac tissue, and multiple treatment-induced processes, which correlated with therapy type and duration. Exogenous sources, including treatment, underpinned, on average, more than 40% of mutations in liver but less than 10% of mutations in brain samples. Finally, we observed tissue-specific selection, with positive selection in tissues such as lung (PTEN and PIK3CA), liver (NF2L2) and spleen (BRAF and NOTCH2), and limited selection in others, such as brain and cardiac tissue. More than 25% of driver mutations in normal tissue exposed to systemic anti-cancer therapy, including in TP53, could be attributed to treatment. Immunotherapy, although not associated with increased mutagenesis, was linked to driver mutations in PPM1D and TP53, illustrating how non-mutagenic treatment can sculpt somatic evolution. Our study reveals the rich tapestry of mutational processes and driver mutations in normal tissue, and the profound effect of lifetime exposures, including cancer treatment, on somatic evolution.

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Conflict of interest statement

Competing interests: M.G.K. has undertaken advisory boards or consultancy for Astellas, Bayer, Guardant Health, Janssen, Roche and Seattle Genetics; is a scientific advisory board (SAB) member for Zai Lab; has received travel expenses from BMS, Janssen, Roche and Zai lab; has received research funding from Novartis and Roche; and has received speaker fees from BMS, Eisai, Janssen and Roche. D.M. reports speaker fees from AstraZeneca, Eli Lilly, BMS and Takeda, consultancy fees from AstraZeneca, Thermo Fisher, Takeda, Amgen, Janssen, MIM Software, Bristol Myers Squibb, Boehringer Ingelheim and Eli Lilly, and has received educational support from Takeda and Amgen. C.S. acknowledges grants from AstraZeneca, Boehringer Ingelheim, Bristol Myers Squibb, Pfizer, Roche-Ventana, Invitae (previously Archer Dx Inc. collaboration in minimal residual disease sequencing technologies), Ono Pharmaceutical and Personalis. C.S. is chief investigator for the AZ MeRmaiD 1 and 2 clinical trials and is the Steering Committee Chair; and co-chief investigator of the NHS Galleri trial funded by GRAIL and a paid member of GRAIL’s SAB. C.S. receives consultant fees from Achilles Therapeutics (and is a SAB member), Bicycle Therapeutics (and is a SAB member), Genentech, Medicxi, China Innovation Centre of Roche (CICoR) formerly Roche Innovation Centre–Shanghai, Metabomed (until July 2022), Relay Therapeutics (and is a SAB member), Saga Diagnostics (and is a SAB member) and the Sarah Cannon Research Institute. C.S. has received honoraria from Amgen, AstraZeneca, Bristol Myers Squibb, GlaxoSmithKline, Illumina, MSD, Novartis, Pfizer and Roche-Ventana. C.S. has previously held stock options in Apogen Biotechnologies and GRAIL, and currently has stock options in Epic Bioscience, Bicycle Therapeutics, Relay Therapeutics, and has stock options and is co-founder of Achilles Therapeutics. C.S. declares a patent application for methods in lung cancer (PCT/US2017/028013); targeting neoantigens (PCT/EP2016/059401); identifying patent response to immune checkpoint blockade (PCT/EP2016/071471); methods for lung cancer detection (US20190106751A1); identifying patients who respond to cancer treatment (PCT/GB2018/051912); determining HLA LOH (PCT/GB2018/052004); predicting survival rates of patients with cancer (PCT/GB2020/050221), and methods and systems for tumour monitoring (PCT/EP2022/077987). C.S. is an inventor on a European patent application (PCT/GB2017/053289) relating to assay technology to detect tumour recurrence. This patent has been licensed to a commercial entity under their terms of employment C.S. is due a revenue share of any revenue generated from such license(s). M.J.-H. has received funding from CRUK, NIH National Cancer Institute, IASLC International Lung Cancer Foundation, Lung Cancer Research Foundation, Rosetrees Trust, UKI NETs and NIHR. M.J.-H. has consulted for Astex Pharmaceutical and Achilles Therapeutics, and is a member of the Achilles Therapeutics SAB and steering committee, has received speaker honoraria from Pfizer, Astex Pharmaceuticals, Oslo Cancer Cluster, Bristol Myers Squibb and Genentech. M.J.-H. is listed as a co-inventor on a European patent application relating to methods to detect lung cancer PCT/US2017/028013—this patent has been licensed to commercial entities and, under terms of employment, M.J.-H. is due a share of any revenue generated from such license(s), and is also listed as a co-inventor on the GB priority patent application (GB2400424.4) with title: Treatment and Prevention of Lung Cancer. N.M. holds patents related to determining HLA LOH (PCT/GB2018/052004), determination of B cell fraction in mixed samples (PCT/EP2024/062999), determination of lymphocyte abundance in mixed samples (PCT/EP2022/070694), identifying responders to cancer treatment (PCT/GB2018/051912), targeting neoantigens (PCT/EP2016/059401), identifying patient response to immune checkpoint blockade (PCT/EP2016/071471), and predicting survival rates of patients with cancer (PCT/GB2020/050221), and has a patent pending in determining HLA disruption (PCT/EP2023/059039). The remaining authors declare no competing interests.

References

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Somatic evolution following cancer treatment in normal tissue

Collaborators

Affiliations

Somatic evolution following cancer treatment in normal tissue

Authors

Collaborators

Affiliations

Abstract

Conflict of interest statement

References

LinkOut - more resources

Full Text Sources

Research Materials

Miscellaneous