Tracking the Evolution of Non–Small-Cell Lung Cancer
Open accessAbstract
BACKGROUND: Among patients with non-small-cell lung cancer (NSCLC), data on intratumor heterogeneity and cancer genome evolution have been limited to small retrospective cohorts. We wanted to prospectively investigate intratumor heterogeneity in relation to clinical outcome and to determine the clonal nature of driver events and evolutionary processes in early-stage NSCLC. METHODS: In this prospective cohort study, we performed multiregion whole-exome sequencing on 100 early-stage NSCLC tumors that had been resected before systemic therapy. We sequenced and analyzed 327 tumor regions to define evolutionary histories, obtain a census of clonal and subclonal events, and assess the relationship between intratumor heterogeneity and recurrence-free survival. RESULTS: ), which remained significant in multivariate analysis. CONCLUSIONS: Intratumor heterogeneity mediated through chromosome instability was associated with an increased risk of recurrence or death, a finding that supports the potential value of chromosome instability as a prognostic predictor. (Funded by Cancer Research UK and others; TRACERx ClinicalTrials.gov number, NCT01888601 .).
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CIN correlates with tumor metastasis.
“Chromosomal instability (CIN) correlates with tumor metastasis1,2”
From Chromosomal instability drives metastasis through a cytosolic DNA response (2018) · cites this paper as [1]
The Results passage (page not available in our copy) links a high proportion of subclonal copy-number alterations to a higher risk of recurrence or death in patients with non–small-cell lung cancer. The Discussion describes copy-number heterogeneity in relation to chromosomal instability, but neither passage establishes a correlation with metastasis specifically. (LLM, conf=0.84)
Experimental — accuracy not yet measuredEntotic invasion has been suggested to favor aneuploidization and polyploidization through cytokinesis failure of engulfing cells.
“entotic invasion has also been suggested to favor aneuploidization and polyploidization (which promote tumor progression) [711–713] through a mechanism involving cytokinesis failure of engulfing cells [714, 715].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [711]
In the TRACERx study, multiregion sequencing of 100 early-stage NSCLCs measured the extent of clonal driver events (1-18 in LUAD and 1-14 in LUSC) and sub-clonal driver events (0-10 in LUAD and 0-12 in LUSC) and established a catalog of clonal alterations.
“In the landmark TRACERx study, multiregion sequencing of 100 early-stage NSCLCs provided a measure of the extent of clonal driver events (1–18 in LUAD and 1–14 in LUSC) and sub-clonal driver events (0–10 in LUAD and 0–12 in LUSC) and established a catalog of clonal alterations74.”
From Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy (2019) · cites this paper as [74]
TP53 mutational inactivation is a clonal and predominantly early event in established NSCLC that precedes genome doubling and subsequent branched evolution.
“This notion is further supported by identification of TP53 mutational inactivation as a clonal and predominantly early event in established NSCLC that precedes genome doubling and subsequent branched evolution74, 103.”
From Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy (2019) · cites this paper as [74]
The tumor genetic landscape can shape anti-tumor immunity, and the immune microenvironment can reciprocally affect tumor genetic evolution.
“While the genetic landscape of tumor can help shape anti-tumor immunity, the immune microenvironment may reciprocally impact the tumor genetic evolution”
From Hallmarks of response, resistance, and toxicity to immune checkpoint blockade (2021) · cites this paper as Jamal-Hanjani et al., 2017
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DeBlasi, J. M., Falzone, A., Caldwell, S., Prieto-Farigua, N., Prigge, J. R., Schmidt, E. E., Chio, I. I. C., Karreth, F. A., & DeNicola, G. M. (2023) · Cancer Research · doi:10.1158/0008-5472.can-22-3848 · Cited by 49 · see citing works
“…are consistent with recent results from the TRACERxstudy,where KEAP1 mutationswerefoundtobeaninitiating driver together with KRAS and TP53 mutations in lung adenocarcinoma (63), and suggest that additional genetic events may be needed to overcome NRF2-mediated inhibition of tumor progression.”
Mitra, A., Andrews, M. C., Roh, W., De Macedo, M. P., Hudgens, C. W., Carapeto, F., Singh, S., Reuben, A., Wang, F., Mao, X., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15538-9 · Cited by 27 · see citing works
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- Authors
- Jamal-Hanjani, M., Wilson, G. A., McGranahan, N., Birkbak, N. J., Watkins, T. B. K., Veeriah, S., Shafi, S., Johnson, D. H., Mitter, R., Rosenthal, R., Salm, M., Horswell, S., Escudero, M., Matthews, N., Rowan, A., Chambers, T., Moore, D. A., Turajlic, S., Xu, H., Lee, S.-M., Forster, M. D., Ahmad, T., Hiley, C. T., Abbosh, C., Falzon, M., Borg, E., Marafioti, T., Lawrence, D., Hayward, M., Kolvekar, S., Panagiotopoulos, N., Janes, S. M., Thakrar, R., Ahmed, A., Blackhall, F., Summers, Y., Shah, R., Joseph, L., Quinn, A. M., Crosbie, P. A., Naidu, B., Middleton, G., Langman, G., Trotter, S., Nicolson, M., Remmen, H., Kerr, K., Chetty, M., Gomersall, L., Fennell, D. A., Nakas, A., Rathinam, S., Anand, G., Khan, S., Russell, P., Ezhil, V., Ismail, B., Irvin-Sellers, M., Prakash, V., Lester, J. F., Kornaszewska, M., Attanoos, R., Adams, H., Davies, H., Dentro, S., Taniere, P., O’Sullivan, B., Lowe, H. L., Hartley, J. A., Iles, N., Bell, H., Ngai, Y., Shaw, J. A., Herrero, J., Szallasi, Z., Schwarz, R. F., Stewart, A., Quezada, S. A., Le Quesne, J., Van Loo, P., Dive, C., Hackshaw, A., & Swanton, C.
- Affiliations
- Cancer Research UK (GB)
- University of Leicester (GB)
- The Francis Crick Institute (GB)
- Aberdeen Royal Infirmary (GB)
- University Hospital of Wales (GB)
- Queen Elizabeth Hospital Birmingham (GB)
- Max Delbrück Center (DE)
- ORCID
- Wilson, Gareth A.
- McGranahan, Nicholas
- Birkbak, Nicolai J.
- Watkins, Thomas B.K.
- Veeriah, Selvaraju
- Johnson, Diana H.
- Mitter, Richard
- Rosenthal, Rachel
- Salm, Max
- Horswell, Stuart
- Escudero, Mickael
- Matthews, Nik
- Rowan, Andrew
- Moore, David A.
- Turajlic, Samra
- Xu, Hang
- Lee, Siow-Ming
- Forster, Martin D.
- Hiley, Crispin T.
- Abbosh, Christopher
- Falzon, Mary
- Borg, Elaine
- Marafioti, Teresa
- Lawrence, David
- Panagiotopoulos, Nikolaos
- Janes, Sam M.
- Thakrar, Ricky
- Blackhall, Fiona
- Summers, Yvonne
- Shah, Rajesh
- Naidu, Babu
- Middleton, Gary
- Fennell, Dean A.
- Nakas, Apostolos
- Rathinam, Sridhar
- Khan, Sajid
- Prakash, Vineet
- Lester, Jason F.
- Davies, Helen
- Dentro, Stefan
- Lowe, Helen L.
- Hartley, John A.
- Shaw, Jacqui A.
- Herrero, Javier
- Schwarz, Roland F.
- Stewart, Aengus
- Quezada, Sergio A.
- Dive, Caroline
- Hackshaw, Allan
- Swanton, Charles
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2017-06
- Volume
- 376
- Issue
- 22
- Pages
- 2109-2121
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- OpenAlex
- W2609243345
- Cited by
- 2,349
- References
- 29
- Citations by year
- 2026: 161 · 2025: 177 · 2024: 207 · 2023: 250 · 2022: 307 · 2021: 331 · 2020: 331 · 2019: 263 · 2018: 231 · 2017: 84 · 2016: 1
- FWCI
- 83.22
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- University of Birmingham Research Portal (University of Birmingham) (publishedVersion, other-oa)
- Research Explorer (The University of Manchester) (publishedVersion, other-oa)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- IRIS (submittedVersion)
- Leicester Research Archive (University of Leicester) (submittedVersion, other-oa)
- Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion)
- Semmelweis University Repository (Semmelweis University) (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- Wellcome Trust (107963/Z/15/Z)
- Francis Crick Institute (10169, 10002, 10202)
- Cancer Research UK (20274, 19740, 19278, 23896, 18892, 20466, 17891, 15951, 20613, 18176, 20276, 20275, 21999, 17786, 22246, 20265, 20465, 22795)
- National Institute for Health and Care Research (CL-2015-17-002, CL-2015-18-009)
- Rosetrees Trust (M35-F2, M35-F1-CD1, M510-CD1)
- Novo Nordisk Fonden (NNF15OC0016584)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Diagnosis and Treatment
- Keywords
- non-small cell lung cancer, intratumoral heterogeneity, tumor evolution, clonal evolution, driver mutations, chromosomal instability, early-stage lung cancer, recurrence-free survival, prognostic factors
- MeSH terms
- Carcinoma, Non-Small-Cell Lung, Female, Humans, Lung Neoplasms, Male, Mutation, Neoplasm Recurrence, Local, Phylogeny, Prognosis, Prospective Studies, Risk Factors, Sequence Analysis, DNA, Disease-Free Survival, Genetic Heterogeneity, Evolution, Molecular, Chromosomal Instability, DNA Copy Number Variations, Exome
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