Lung adenocarcinoma promotion by air pollutants
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Abstract
A complete understanding of how exposure to environmental substances promotes cancer formation is lacking. More than 70 years ago, tumorigenesis was proposed to occur in a two-step process: an initiating step that induces mutations in healthy cells, followed by a promoter step that triggers cancer development1. Here we propose that environmental particulate matter measuring ≤2.5 μm (PM2.5), known to be associated with lung cancer risk, promotes lung cancer by acting on cells that harbour pre-existing oncogenic mutations in healthy lung tissue. Focusing on EGFR-driven lung cancer, which is more common in never-smokers or light smokers, we found a significant association between PM2.5 levels and the incidence of lung cancer for 32,957 EGFR-driven lung cancer cases in four within-country cohorts. Functional mouse models revealed that air pollutants cause an influx of macrophages into the lung and release of interleukin-1β. This process results in a progenitor-like cell state within EGFR mutant lung alveolar type II epithelial cells that fuels tumorigenesis. Ultradeep mutational profiling of histologically normal lung tissue from 295 individuals across 3 clinical cohorts revealed oncogenic EGFR and KRAS driver mutations in 18% and 53% of healthy tissue samples, respectively. These findings collectively support a tumour-promoting role for PM2.5 air pollutants and provide impetus for public health policy initiatives to address air pollution to reduce disease burden. Combination of epidemiology, preclinical models and ultradeep DNA profiling of clinical cohorts unpicks the inflammatory mechanism by which air pollution promotes lung cancer
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A novel mechanism has been proposed on the underlying means by which air pollution causes adenocarcinoma.
“Previous epidemiological studies have linked the high burden of adenocarcinoma to long-term exposure to outdoor air pollution in transitioned countries [30][31][32] ; and, recently, a novel mechanism has been proposed on the underlying means by which air pollution causes adenocarcinoma.33”
From Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. (2024) · cites this paper as [33]
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Ryu, M. H. (2022) · cIRcle (University of British Columbia) · doi:10.14288/1.0398486 · Cited by 1 · see citing works
Self-citation
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- [7]WHO Global Air Quality Guidelines Particulate Matter (PM2.5 and PM10), Ozone, Nitrogen Dioxide, Sulfur Dioxide and Carbon Monoxide World Health Organization 2021 34662007
- [39]IARC Working Group on the – Evaluation of Carcinogenic Risks to Humans IARC Monograph Diesel And Gasoline Engine Exhausts And Some Nitroarenes World Health Organization 2014 105 PMC4781216 26442290
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Cited by
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Bray, F., Laversanne, M., Sung, H., Ferlay, J., Siegel, R. L., Soerjomataram, I., & Jemal, A. (2024) · CA: a cancer journal for clinicians · doi:10.3322/caac.21834 · Cited by 27,064 · see citing works
“33 Thus the high levels of air pollution recorded in several urban areas worldwide may be among the important underlying reasons for the observed patterns of lung cancer.”
BackgroundExposure to Air Pollution, Genetic Susceptibility, and Psoriasis Risk in the UK
Wu, J., Ma, Y., Yang, J., & Tian, Y. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2024.21665 · Cited by 38 · see citing works
Du, X., Xu, X., Dong, X.-X., Liang, X., Wu, Y., Du, Z., Pan, C.-W., Liang, G., Li, Y.-Z., Zheng, Y.-J., et al. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.5c01138 · Cited by 24 · see citing works
Distribution and characteristics of malignant tumours by lung lobe
Nilssen, Y., Brustugun, O. T., Fjellbirkeland, L., Helland, Å., Møller, B., Wahl, S. G. F., & Solberg, S. (2024) · BMC Pulmonary Medicine · doi:10.1186/s12890-024-02918-w · Cited by 11 · see citing works
“Further, Hill et al. have recently described the significance of air pollut-ants in inducing EGFR-driven ACs in never smokers [22].”
Background
- Authors
- Hill, W., Lim, E. L., Weeden, C. E., Lee, C., Augustine, M., Chen, K., Kuan, F.-C., Marongiu, F., Evans, E. J., Moore, D. A., Rodrigues, F. S., Pich, O., Bakker, B., Cha, H., Myers, R., van Maldegem, F., Boumelha, J., Veeriah, S., Rowan, A., Naceur-Lombardelli, C., Karasaki, T., Sivakumar, M., De, S., Caswell, D. R., Nagano, A., Black, J. R. M., Martínez-Ruiz, C., Ryu, M. H., Huff, R. D., Li, S., Favé, M.-J., Magness, A., Suárez-Bonnet, A., Priestnall, S. L., Lüchtenborg, M., Lavelle, K., Pethick, J., Hardy, S., McRonald, F. E., Lin, M.-H., Troccoli, C. I., Ghosh, M., Miller, Y. E., Merrick, D. T., Keith, R. L., Al Bakir, M., Bailey, C., Hill, M. S., Saal, L. H., Chen, Y., George, A. M., Abbosh, C., Kanu, N., Lee, S.-H., McGranahan, N., Berg, C. D., Sasieni, P., Houlston, R., Turnbull, C., Lam, S., Awadalla, P., Grönroos, E., Downward, J., Jacks, T., Carlsten, C., Malanchi, I., Hackshaw, A., Litchfield, K., TRACERx Consortium, Lester, J. F., Bajaj, A., Nakas, A., Sodha-Ramdeen, A., Ang, K., Tufail, M., Chowdhry, M. F., Scotland, M., Boyles, R., Rathinam, S., Wilson, C., Marrone, D., Dulloo, S., Fennell, D. A., Matharu, G., Shaw, J. A., Riley, J., Primrose, L., Boleti, E., Cheyne, H., Khalil, M., Richardson, S., Cruickshank, T., Price, G., Kerr, K. M., Benafif, S., Gilbert, K., Naidu, B., Patel, A. J., Osman, A., Lacson, C., Langman, G., Shackleford, H., Djearaman, M., Kadiri, S., Middleton, G., Leek, A., Hodgkinson, J. D., Totten, N., Montero, A., Smith, E., Fontaine, E., Granato, F., Doran, H., Novasio, J., Rammohan, K., Joseph, L., Bishop, P., Shah, R., Moss, S., Joshi, V., Crosbie, P., Gomes, F., Brown, K., Carter, M., Chaturvedi, A., Priest, L., Oliveira, P., Lindsay, C. R., Blackhall, F. H., Krebs, M. G., Summers, Y., Clipson, A., Tugwood, J., Kerr, A., Rothwell, D. G., Kilgour, E., Dive, C., Aerts, H. J. W. L., Schwarz, R. F., Kaufmann, T. L., Wilson, G. A., Rosenthal, R., Van Loo, P., Birkbak, N. J., Szallasi, Z., Kisistok, J., Sokac, M., Salgado, R., Diossy, M., Demeulemeester, J., Bunkum, A., Stewart, A., Frankell, A. M., Karamani, A., Toncheva, A., Huebner, A., Chain, B., Campbell, B. B., Castignani, C., Puttick, C., Richard, C., Hiley, C. T., Pearce, D. R., Karagianni, D., Biswas, D., Levi, D., Hoxha, E., Cadieux, E. L., Colliver, E., Nye, E., Gálvez-Cancino, F., Athanasopoulou, F., Gimeno-Valiente, F., Kassiotis, G., Stavrou, G., Mastrokalos, G., Zhai, H., Lowe, H. L., Matos, I. G., Goldman, J., Reading, J. L., Herrero, J., Rane, J. K., Nicod, J., Lam, J. M., Hartley, J. A., Peggs, K. S., Enfield, K. S. S., Selvaraju, K., Thol, K., Ng, K. W., Dijkstra, K., Grigoriadis, K., Thakkar, K., Ensell, L., Shah, M., Duran, M. V., Litovchenko, M., Sunderland, M. W., Dietzen, M., Leung, M., Escudero, M., Angelova, M., Tanić, M., Chervova, O., Lucas, O., Al-Sawaf, O., Prymas, P., Hobson, P., Pawlik, P., Stone, R. K., Bentham, R., Hynds, R. E., Vendramin, R., Saghafinia, S., López, S., Gamble, S., Ung, S. K. A., Quezada, S. A., Vanloo, S., Zaccaria, S., Hessey, S., Ward, S., Boeing, S., Beck, S., Bola, S. K., Denner, T., Marafioti, T., Mourikis, T. P., Watkins, T. B. K., Spanswick, V., Barbè, V., Lu, W.-T., Liu, W. K., Wu, Y., Naito, Y., Ramsden, Z., Veiga, C., Royle, G., Collins-Fekete, C.-A., Fraioli, F., Ashford, P., Clark, T., Forster, M. D., Lee, S. M., Borg, E., Falzon, M., Papadatos-Pastos, D., Wilson, J., Ahmad, T., Procter, A. J., Ahmed, A., Taylor, M. N., Nair, A., Lawrence, D., Patrini, D., Navani, N., Thakrar, R. M., Janes, S. M., Hoogenboom, E. M., Monk, F., Holding, J. W., Choudhary, J., Bhakhri, K., Scarci, M., Hayward, M., Panagiotopoulos, N., Gorman, P., Khiroya, R., Stephens, R. C. M., Wong, Y. N. S., Bandula, S., Sharp, A., Smith, S., Gower, N., Dhanda, H. K., Chan, K., Pilotti, C., Leslie, R., Grapa, A., Zhang, H., AbdulJabbar, K., Pan, X., Yuan, Y., Chuter, D., MacKenzie, M., Chee, S., Alzetani, A., Cave, J., Scarlett, L., Richards, J., Ingram, P., Austin, S., Lim, E., De Sousa, P., Jordan, S., Rice, A., Raubenheimer, H., Bhayani, H., Ambrose, L., Devaraj, A., Chavan, H., Begum, S., Buderi, S. I., Kaniu, D., Malima, M., Booth, S., Nicholson, A. G., Fernandes, N., Shah, P., Proli, C., Hewish, M., Danson, S., Shackcloth, M. J., Robinson, L., Russell, P., Blyth, K. G., Dick, C., Le Quesne, J., Kirk, A., Asif, M., Bilancia, R., Kostoulas, N., Thomas, M., DeGregori, J., Jamal-Hanjani, M., & Swanton, C.
- Affiliations
- The Francis Crick Institute (GB)
- Peking University People's Hospital (CN)
- Chang Gung University (TW)
- University of Cagliari (IT)
- University of Colorado Anschutz (US)
- University College Hospital (GB)
- Samsung Medical Center (KR)
- University of British Columbia (CA)
- University College London (GB)
- Cancer Research UK (GB)
- Ontario Institute for Cancer Research (CA)
- Royal Veterinary College (GB)
- King's College London (GB)
- NHS England (GB)
- Chang Gung Memorial Hospital (TW)
- VA Eastern Colorado Health Care System (US)
- Lund University (SE)
- Institute of Cancer Research (GB)
- Koch Institute for Integrative Cancer Research At MIT (US)
- Swansea Bay University Health Board (GB)
- University Hospitals of Leicester NHS Trust (GB)
- University of Leicester (GB)
- Royal Free London NHS Foundation Trust (GB)
- Aberdeen Royal Infirmary (GB)
- University of Aberdeen (GB)
- Whittington Hospital (GB)
- University of Birmingham (GB)
- University Hospitals Birmingham NHS Foundation Trust (GB)
- Cancer Research UK Manchester Centre (GB)
- Manchester University NHS Foundation Trust (GB)
- University of Manchester (GB)
- The Christie NHS Foundation Trust (GB)
- Brigham and Women's Hospital (US)
- University of Cologne (DE)
- Max Delbrück Center (DE)
- Aarhus University (DK)
- Peter MacCallum Cancer Centre (AU)
- The Netherlands Cancer Institute (NL)
- Institute of Structural and Molecular Biology (GB)
- The University of Texas MD Anderson Cancer Center (US)
- University Hospital Southampton NHS Foundation Trust (GB)
- Guy's and St Thomas' NHS Foundation Trust (GB)
- Royal Surrey County Hospital (GB)
- Sheffield Teaching Hospitals NHS Foundation Trust (GB)
- Liverpool Heart and Chest Hospital (GB)
- Princess Alexandra Hospital NHS Trust (GB)
- Cancer Research UK Scotland Institute (GB)
- NHS Greater Glasgow and Clyde (GB)
- Golden Jubilee National Hospital (GB)
- Corresponding author
- Swanton, Charles
- ORCID
- Hill, William
- Lim, Emilia L.
- Weeden, Clare E.
- Lee, Claudia
- Augustine, Marcellus
- Chen, Kezhong
- Kuan, Feng-Che
- Marongiu, Fabio
- Evans, Edward J.
- Moore, David A.
- Rodrigues, Felipe S.
- Pich, Oriol
- Bakker, Bjorn
- Cha, Hongui
- Myers, Renelle
- Boumelha, Jesse
- Veeriah, Selvaraju
- Rowan, Andrew
- Karasaki, Takahiro
- Sivakumar, Monica
- De, Swapnanil
- Caswell, Deborah R.
- Nagano, Ai
- Black, James R. M.
- Martínez-Ruiz, Carlos
- Ryu, Min Hyung
- Huff, Ryan D.
- Li, Shijia
- Favé, Marie-Julie
- Magness, Alastair
- Suárez-Bonnet, Alejandro
- Priestnall, Simon L.
- Lüchtenborg, Margreet
- Lavelle, Katrina
- Pethick, Joanna
- McRonald, Fiona E.
- Lin, Meng-Hung
- Troccoli, Clara I.
- Ghosh, Moumita
- Merrick, Daniel T.
- Keith, Robert L.
- Al Bakir, Maise
- Bailey, Chris
- Hill, Mark S.
- Saal, Lao H.
- Chen, Yilun
- George, Anthony M.
- Abbosh, Christopher
- Kanu, Nnennaya
- Lee, Se-Hoon
- McGranahan, Nicholas
- Berg, Christine D.
- Sasieni, Peter
- Houlston, Richard
- Turnbull, Clare
- Lam, Stephen
- Awadalla, Philip
- Grönroos, Eva
- Downward, Julian
- Jacks, Tyler
- Malanchi, Ilaria
- Hackshaw, Allan
- Litchfield, Kevin
- Lester, Jason F.
- Bajaj, Amrita
- Nakas, Apostolos
- Rathinam, Sridhar
- Wilson, Claire
- Marrone, Domenic
- Fennell, Dean A.
- Shaw, Jacqui A.
- Primrose, Lindsay
- Price, Gillian
- Benafif, Sarah
- Naidu, Babu
- Patel, Akshay J.
- Osman, Aya
- Djearaman, Madava
- Middleton, Gary
- Shah, Rajesh
- Moss, Stuart
- Crosbie, Philip
- Brown, Kate
- Carter, Mathew
- Chaturvedi, Anshuman
- Priest, Lynsey
- Oliveira, Pedro
- Lindsay, Colin R.
- Blackhall, Fiona H.
- Krebs, Matthew G.
- Summers, Yvonne
- Clipson, Alexandra
- Kerr, Alastair
- Rothwell, Dominic G.
- Dive, Caroline
- Aerts, Hugo J. W. L.
- Schwarz, Roland F.
- Kaufmann, Tom L.
- Wilson, Gareth A.
- Rosenthal, Rachel
- Birkbak, Nicolai J.
- Salgado, Roberto
- Demeulemeester, Jonas
- Bunkum, Abigail
- Frankell, Alexander M.
- Huebner, Ariana
- Chain, Benny
- Castignani, Carla
- Puttick, Clare
- Richard, Corentin
- Hiley, Crispin T.
- Pearce, David R.
- Karagianni, Despoina
- Biswas, Dhruva
- Levi, Dina
- Cadieux, Elizabeth Larose
- Colliver, Emma
- Nye, Emma
- Gimeno-Valiente, Francisco
- Kassiotis, George
- Stavrou, Georgia
- Lowe, Helen L.
- Matos, Ignacio Garcia
- Goldman, Jacki
- Reading, James L.
- Herrero, Javier
- Rane, Jayant K.
- Lam, Jie Min
- Hartley, John A.
- Peggs, Karl S.
- Enfield, Katey S. S.
- Thol, Kerstin
- Ng, Kevin W.
- Dijkstra, Krijn
- Grigoriadis, Kristiana
- Thakkar, Krupa
- Ensell, Leah
- Litovchenko, Maria
- Sunderland, Mariana Werner
- Dietzen, Michelle
- Leung, Michelle
- Escudero, Mickael
- Angelova, Mihaela
- Tanić, Miljana
- Chervova, Olga
- Lucas, Olivia
- Hobson, Philip
- Pawlik, Piotr
- Bentham, Robert
- Hynds, Robert E.
- Vendramin, Roberto
- Saghafinia, Sadegh
- López, Saioa
- Ung, Seng Kuong Anakin
- Quezada, Sergio A.
- Zaccaria, Simone
- Hessey, Sonya
- Ward, Sophia
- Boeing, Stefan
- Beck, Stephan
- Bola, Supreet Kaur
- Marafioti, Teresa
- Mourikis, Thanos P.
- Watkins, Thomas B. K.
- Barbè, Vittorio
- Lu, Wei-Ting
- Liu, Wing Kin
- Wu, Yin
- Naito, Yutaka
- Veiga, Catarina
- Royle, Gary
- Fraioli, Francesco
- Ashford, Paul
- Forster, Martin D.
- Lee, Siow Ming
- Borg, Elaine
- Falzon, Mary
- Wilson, James
- Procter, Alexander James
- Nair, Arjun
- Lawrence, David
- Patrini, Davide
- Navani, Neal
- Thakrar, Ricky M.
- Janes, Sam M.
- Scarci, Marco
- Panagiotopoulos, Nikolaos
- Stephens, Robert C. M.
- Wong, Yien Ning Sophia
- Bandula, Steve
- Sharp, Abigail
- Smith, Sean
- Dhanda, Harjot Kaur
- Zhang, Hanyun
- AbdulJabbar, Khalid
- Pan, Xiaoxi
- Yuan, Yinyin
- Chee, Serena
- Alzetani, Aiman
- Cave, Judith
- Lim, Eric
- Rice, Alexandra
- Devaraj, Anand
- Begum, Sofina
- Nicholson, Andrew G.
- Fernandes, Nadia
- Danson, Sarah
- Shackcloth, Michael J.
- Kirk, Alan
- Bilancia, Rocco
- Thomas, Mathew
- DeGregori, James
- Jamal-Hanjani, Mariam
- Swanton, Charles
- Venue
- Nature
- Published
- 2023-04-05
- Volume
- 616
- Issue
- 7955
- Pages
- 159-167
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7614604
- OpenAlex
- W4362606390
- Cited by
- 808
- References
- 81
- Citations by year
- 2026: 194 · 2025: 264 · 2024: 248 · 2023: 100 · 2022: 1
- FWCI
- 92.48
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature (publishedVersion, cc-by)
- Research Square (acceptedVersion, cc-by)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, cc-by)
- Pure Amsterdam UMC (publishedVersion, cc-by)
- Research Explorer (The University of Manchester) (publishedVersion, other-oa)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion, cc-by)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion, cc-by)
- Queen Mary Research Online (Queen Mary University of London) (acceptedVersion, cc-by)
- PubMed Central (acceptedVersion, cc-by)
- Aberdeen University Research Archive (Aberdeen University) (submittedVersion, cc-by)
- UCL Discovery (University College London) (submittedVersion, cc-by)
- UNICA IRIS Institutional Research Information System (University of Cagliari) (submittedVersion, cc-by)
- Lirias (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Lund University Publications (Lund University) (submittedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- American Association for Cancer Research (SU2C-AACR-DT23-17, 18-90-52-DEGR)
- U.S. Department of Veterans Affairs (I01 BX004495)
- Breast Cancer Research Foundation (SU2C-AACR-DT23-17)
- LUNGevity Foundation (SU2C-AACR-DT23-17)
- Amgen
- Bristol-Myers Squibb
- Pfizer
- AstraZeneca
- International Association for the Study of Lung Cancer
- Entertainment Industry Foundation
- European Respiratory Society
- Wellcome Trust (FP7/2007–2013, FC001169, 100034, 16584, CC2041, FC001112, 211179/Z/18/Z, 211179, 103799/A/14/Z)
- Francis Crick Institute (CC2088, FC001112, CC1064, CC2008, CC1119, CC2097, CC1061, FC001169, CC1062, CC2051, CC2041)
- LifeArc
- Génome Québec
- Astex Pharmaceuticals
- Revolution Medicines
- Invitae
- Cancer Research UK (FP7/2007-2013, 25349, 25514, EDDPJT-Nov22/100042, CTRNBC-2022/100001, EDDPMA‐Nov21/100034, ID16584, SEBSTF-2021\100007, 16584, 21999, 17786, CC2041, RCCFEL\100099, FC001169, C69256/A30194, 29569, 30025, FC001112)
- National Institute for Health and Care Research (FP7/2007–2013, CL-2020-18-501, CL-2015-18-009, ACF-2014-18-006)
- Royal Society (211179/Z/18/Z, 211179, RP/EA/180007)
- University College London
- European Commission (665233, 2007–2013, FP7 2007-2013, HORIZON2020, H2020, FP7/2007, 607722, 835297)
- Rosetrees Trust (FP7/2007-2013, PGL21 10119, ID16584, M35-F2, A2437, OoR2020 100009)
- National Research Foundation
- National Natural Science Foundation of China (No.82072566, FP7/2007-2013, FP7/2007, 82072566)
- Cancerfonden
- Korea Health Industry Development Institute (HR20C0025)
- National Research Foundation of Korea (HR20C0025, 2020R1A2C3006535)
- Vetenskapsrådet (FP7/2007-2013)
- Chang Gung Medical Foundation
- Chinese Academy of Medical Sciences (2021RU002)
- Peking University (RS2019-01)
- University College London Hospitals NHS Foundation Trust
- Ono Pharmaceutical
- Ministry of Science and ICT, South Korea (HR20C0025)
- Peking University People's Hospital (RS2019-01)
- National Institutes of Health (FP7/2007-2013, H2020, P 30CA046934)
- Genentech
- Stand Up To Cancer (SU2C-AACRDT23-17, AACR-DT23-17)
- Horizon 2020 Framework Programme (FP7/2007-2013, 665233, 835297)
- Medical Research Council (FP7/20072013, MR/P014712/1, MR/V033077/1, FC001112, MR/W025051/1, MC_PC_17228, FC001169)
- Engineering and Physical Sciences Research Council (EP/X030059/1)
- Japan Society for the Promotion of Science (202060447, 052004)
- National Human Genome Research Institute
- National Cancer Institute (T32CA174648, CA190216, R01CA219893, P30CA046934, T32CA190216)
- H2020 European Research Council (725492)
- FP7 Ideas: European Research Council (617844)
- Linda Crnic Institute for Down Syndrome, University of Colorado School of Medicine, Anschutz Medical Campus
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Occupational and environmental lung diseases
- Keywords
- lung adenocarcinoma, PM2.5, air pollution, tumor promotion, EGFR mutation, KRAS mutation, alveolar type II cells, macrophage infiltration, IL-1β, lung inflammation, never smokers, environmental carcinogenesis
- MeSH terms
- Adenocarcinoma of Lung, Air Pollutants, Air Pollution, Animals, Cell Transformation, Neoplastic, Environmental Exposure, Lung Neoplasms, Particle Size, Cohort Studies, Macrophages, Alveolar, Mice, Particulate Matter, Interleukin-1beta, Alveolar Epithelial Cells, ErbB Receptors
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