375
Views
3
CrossRef citations to date
0
Altmetric
Articles

Ambient PM2.5 exposure causes cellular senescence via DNA damage, micronuclei formation, and cGAS activation

, , ORCID Icon, , , , , , & ORCID Icon show all
Pages 757-775 | Received 21 Jul 2022, Accepted 09 Nov 2022, Published online: 20 Nov 2022

References

  • Abbas, I., G. Garcon, F. Saint-Georges, V. Andre, P. Gosset, S. Billet, J. Le Goff, A. Verdin, et al. 2013. “Polycyclic Aromatic Hydrocarbons within Airborne Particulate Matter (PM2.5) Produced DNA Bulky Stable Adducts in a Human Lung Cell Coculture Model.” Journal of Applied Toxicology 33 (2): 109–119. http://dx.doi.org/10.1002/jat.1722.
  • Ablasser, A., M. Goldeck, T. Cavlar, T. Deimling, G. Witte, I. Rohl, K. P. Hopfner, J. Ludwig, et al. 2013. “cGAS Produces a 2 '-5 '-Linked Cyclic Dinucleotide Second Messenger That Activates STING.” Nature 498 (7454): 380–384. http://dx.doi.org/10.1038/nature12306.
  • Araviiskaia, E., E. Berardesca, T. Bieber, G. Gontijo, M. S. Viera, L. Marrot, B. Chuberre, and B. Dreno. 2019. “The Impact of Airborne Pollution on Skin.” Journal of the European Academy of Dermatology and Venereology 33 (8): 1496–1505. http://dx.doi.org/10.1111/jdv.15583.
  • Baker, D. J., B. G. Childs, M. Durik, M. E. Wijers, C. J. Sieben, J. Zhong, R. A. Saltness, K. B. Jeganathan, et al. 2016. “Naturally Occurring p16(Ink4a)-Positive Cells Shorten Healthy Lifespan.” Nature 530 (7589): 184–189. http://dx.doi.org/10.1038/nature16932.
  • Childs, B. G., D. J. Baker, T. Wijshake, C. A. Conover, J. Campisi, and J. M. Van Deursen. 2016. “Senescent Intimal Foam Cells Are Deleterious at All Stages of Atherosclerosis.” Science 354 (6311): 472–477. http://dx.doi.org/10.1126/science.aaf6659.
  • Clay, D. E., H. S. Bretscher, E. A. Jezuit, K. B. Bush, and D. T. Fox. 2021. “Persistent DNA Damage Signaling and DNA Polymerase Theta Promote Broken Chromosome Segregation.” Journal of Cell Biology 220 (12): e202106116. http://dx.doi.org/10.1083/jcb.202106116
  • Demaria, M., M. N. O'leary, J. H. Chang, L. J. Shao, S. Liu, F. Alimirah, K. Koenig, C. Le, et al. 2017. “Cellular Senescence Promotes Adverse Effects of Chemotherapy and Cancer Relapse.” Cancer Discovery 7 (2): 165–176. http://dx.doi.org/10.1158/2159-8290.Cd-16-0241.
  • Di Domenico, M., S. G. D. Benevenuto, P. P. Tomasini, V. Y. Yariwake, N. D. Alves, F. L. Rahmeier, M. D. Fernandes, D. J. Moura, et al. 2020. “Concentrated Ambient Fine Particulate Matter (PM2.5) Exposure Induce Brain Damage in Pre and Postnatal Exposed Mice.” Neurotoxicology 79: 127–141. http://dx.doi.org/10.1016/j.neuro.2020.05.004.
  • Feng, Y. L., Q. Liu, R. D. Chen, S. C. Liu, Z. C. Huang, K. M. Liu, X. Y. Yang, and A. Y. Xie. 2022. “DNA Nicks Induce Mutational Signatures Associated with BRCA1 Deficiency.” Nature Communications 13 (1): 4285. http://dx.doi.org/10.1038/s41467-022-32011-x.
  • Forouzanfar, M. H., A. Afshin, L. T. Alexander, H. R. Anderson, Z. A. Bhutta, S. Biryukov, M. Brauer, R. Burnett, et al. 2016. “Global, Regional, and National Comparative Risk Assessment of 79 Behavioural, Environmental and Occupational, and Metabolic Risks or Clusters of Risks, 1990–2015: A Systematic Analysis for the Global Burden of Disease Study 2015.” The Lancet 388 (10053): 1659–1724. http://dx.doi.org/10.1016/S0140-6736(16)31679-8
  • Guo, Q., X. Chen, J. Chen, G. Zheng, C. Xie, H. Wu, Z. Miao, Y. Lin, et al. 2021b. “STING Promotes Senescence, Apoptosis, and Extracellular Matrix Degradation in Osteoarthritis via the NF-kappaB Signaling Pathway.” Cell Death & Disease 12 (1): 13. http://dx.doi.org/10.1038/s41419-020-03341-9.
  • Hatch, E. M., A. H. Fischer, T. J. Deerinck, and M. W. Hetzer. 2013. “Catastrophic Nuclear Envelope Collapse in Cancer Cell Micronuclei.” Cell 154 (1): 47–60. http://dx.doi.org/10.1016/j.cell.2013.06.007.
  • Herath, M. U. L. H., M. J. Piao, K. A. Kang, A. X. Zhen, P. D. S. M. Fernando, H. K. Kang, J. M. Yi, and, J. W. Hyun. 2022. “Hesperidin Exhibits Protective Effects against PM2.5-Mediated Mitochondrial Damage, Cell Cycle Arrest, and Cellular Senescence in Human HaCaT Keratinocytes.” Molecules 27 (15): 4800. http://dx.doi.org/10.3390/molecules27154800
  • Hintzsche, H., U. Hemmann, A. Poth, D. Utesch, J. Lott, and H. Stopper, Working Group “In vitro micronucleus test”, Gesellschaft für Umwelt-Mutationsforschung (GUM, German-speaking section of the European Environmental Mutagenesis and Genomics Society EEMGS). 2017. “Fate of Micronuclei and Micronucleated Cells.” Mutation Research. Reviews in Mutation Research 771: 85–98. http://dx.doi.org/10.1016/j.mrrev.2017.02.002.
  • Huijser, E., I. L. A. Bodewes, M. S. Lourens, C. G. van Helden-Meeuwsen, T. P. P. van den Bosch, D. G. B. Grashof, H. J. G. van de Werken, et al. 2022. “Hyperresponsive Cytosolic DNA-Sensing Pathway in Monocytes from Primary Sjogren’s Syndrome.” Rheumatology 61 (8): 3491–3496. http://dx.doi.org/10.1093/rheumatology/keac016
  • Kamal, N. S. M., S. Safuan, S. Shamsuddin, and P. Foroozandeh. 2020. “Aging of the Cells: Insight into Cellular Senescence and Detection Methods.” European Journal of Cell Biology 99 (6): 151108. http://dx.doi.org/10.1016/j.ejcb.2020.151108.
  • Li, L., R. Meng, Y. L. Lei, S. M. Wu, and Y. Jiang. 2022a. “Human Health Risk Assessment of Heavy Metals from PM2.5 in China’s 29 Provincial Capital Cities.” Environmental Science and Pollution Research 29: 63028–63040. http://dx.doi.org/10.1007/s11356-022-20229-7
  • Li, T., and Z. J. Chen. 2018. “The cGAS-cGAMP-STING Pathway Connects DNA Damage to Inflammation, Senescence, and Cancer.” The Journal of Experimental Medicine 215 (5): 1287–1299. http://dx.doi.org/10.1084/jem.20180139.
  • Li, X., C. Yan, C. Wang, J. Ma, W. Li, J. Liu, and Y. Liu. 2022b. “PM2.5-Bound Elements in Hebei Province, China: Pollution Levels, Source Apportionment and Health Risks.” The Science of the Total Environment 806 (Pt 1): 150440. http://dx.doi.org/10.1016/j.scitotenv.2021.150440.
  • Liao, Y., J. Cheng, X. Kong, S. Li, X. Li, M. Zhang, H. Zhang, et al. 2020. “HDAC3 Inhibition Ameliorates Ischemia/Reperfusion-Induced Brain Injury by Regulating the Microglial cGAS-STING Pathway.” Theranostics 10 (21): 9644–9662. http://dx.doi.org/10.7150/thno.47651.
  • Longhin, E., J. A. Holme, K. B. Gutzkow, V. M. Arlt, J. E. Kucab, M. Camatini, and M. Gualtieri. 2013. “Cell Cycle Alterations Induced by Urban PM2.5 in Bronchial Epithelial Cells: Characterization of the Process and Possible Mechanisms Involved.” Particle and Fibre Toxicology 10: 63. http://dx.doi.org/10.1186/1743-8977-10-63.
  • Luo, H. G., R. J. Gu, H. Y. Ouyang, L. H. Wang, S. W. Shi, Y. N. Ji, B. C. Bao, G. Q. Liao, et al. 2021. “Cadmium Exposure Induces Osteoporosis through Cellular Senescence, Associated with Activation of NF-Kappa B Pathway and Mitochondrial Dysfunction.” Environmental Pollution (Barking, Essex: 1987) 290: 118043. http://dx.doi.org/10.1016/j.envpol.2021.118043.
  • Mackenzie, K. J., P. Carroll, C. A. Martin, O. Murina, A. Fluteau, D. J. S. Impson, N. Olova, H. Sutcliffe, et al. 2017. “cGAS Surveillance of Micronuclei Links Genome Instability to Innate Immunity.” Nature 548 (7668): 461–465. http://dx.doi.org/10.1038/nature23449
  • Mann, C. C. D., and P. J. Kranzusch. 2017. “cGAS Conducts Micronuclei DNA Surveillance.” Trends in Cell Biology 27 (10): 697–698. http://dx.doi.org/10.1016/j.tcb.2017.08.007.
  • Ogrodnik, M., H. Salmonowicz, D. Jurk, and J. F. Passos. 2019. “Expansion and Cell-Cycle Arrest: Common Denominators of Cellular Senescence.” Trends in Biochemical Sciences 44 (12): 996–1008. http://dx.doi.org/10.1016/j.tibs.2019.06.011.
  • Paz, M. F. C. J., A. L. P. Sobral, J. N. Picada, I. Grivicich, A. L. Gomes, A. M. O. F. Da Mata, M. V. O. B. De Alencar, R. M. De Carvalho, et al. 2018. “Persistent Increased Frequency of Genomic Instability in Women Diagnosed with Breast Cancer: Before, during, and after Treatments.” Oxidative Medicine and Cellular Longevity 2018: 2846819. http://dx.doi.org/10.1155/2018/2846819.
  • Peng, F., G. Tsuji, J. Z. Zhang, Z. Chen, and M. Furue. 2019. “Potential Role of PM2.5 in Melanogenesis.” Environment International 132: 105063. http://dx.doi.org/10.1016/j.envint.2019.105063.
  • Pons, B. J., A. Pettes-Duler, C. Naylies, F. Taieb, C. Bouchenot, S. Hashim, P. Rouimi, M. Deslande, et al. 2021. “Chronic Exposure to Cytolethal Distending Toxin (CDT) Promotes a cGAS-Dependent Type I Interferon Response.” Cellular and Molecular Life Sciences 78 (17–18): 6319–6335. http://dx.doi.org/10.1007/s00018-021-03902-x
  • Robin, J. D., A. T. Ludlow, K. Batten, F. Magdinier, G. Stadler, K. R. Wagner, J. W. Shay, and W. E. Wright. 2014. “Telomere Position Effect: Regulation of Gene Expression with Progressive Telomere Shortening over Long Distances.” Genes & Development 28 (22): 2464–2476. http://dx.doi.org/10.1101/gad.251041.114.
  • Ryu, Y. S., K. A. Kang, M. J. Piao, M. J. Ahn, J. M. Yi, S. G. Bossi, Y. M. Hyun, C. O. Park, et al. 2019. “Particulate Matter-Induced Senescence of Skin Keratinocytes Involves Oxidative Stress-Dependent Epigenetic Modifications.” Experimental & Molecular Medicine 51 (9): 1–14. http://dx.doi.org/10.1038/s12276-019-0305-4.
  • Schuliga, M., J. Read, K. E. C. Blokland, D. W. Waters, J. Burgess, C. Prele, S. E. Mutsaers, J. Jaffar, et al. 2020. “Self DNA Perpetuates IPF Lung Fibroblast Senescence in a cGAS-Dependent Manner.” Clinical Science (London, England: 1979) 134 (7): 889–905. http://dx.doi.org/10.1042/Cs20191160.
  • Seluanov, A., C. Hine, M. Bozzella, A. Hall, T. H. C. Sasahara, A. aCM Ribeiro, K. C. Catania, D. C. Presgraves, et al. 2008. “Distinct Tumor Suppressor Mechanisms Evolve in Rodent Species That Differ in Size and Lifespan.” Aging Cell 7 (6): 813–823. http://dx.doi.org/10.1111/j.1474-9726.2008.00431.x.
  • Seluanov, A., Z. Mao, and V. Gorbunova. 2010. “Analysis of DNA Double-Strand Break (DSB) Repair in Mammalian Cells.” Journal of Visualized Experiments 8: 2002. http://dx.doi.org/10.3791/2002
  • Sharma, J., K. Parsai, P. Raghuwanshi, S. A. Ali, V. Tiwari, A. Bhargava, and P. K. Mishra. 2021. “Emerging Role of Mitochondria in Airborne Particulate Matter-Induced Immunotoxicity.” Environmental Pollution (Barking, Essex: 1987) 270: 116242. http://dx.doi.org/10.1016/j.envpol.2020.116242
  • Song, X. Y., J. H. Liu, N. B. Geng, Y. C. Shan, B. Q. Zhang, B. F. Zhao, Y. W. Ni, et al. 2022. “Multi-Omics Analysis to Reveal Disorders of Cell Metabolism and Integrin Signaling Pathways Induced by PM2.5.” Journal of Hazardous Materials 424 (Pt C): 127573. http://dx.doi.org/10.1016/j.jhazmat.2021.127573.
  • Swift, M. L., C. Sell, and J. Azizkhan-Clifford. 2022. “DNA Damage-Induced Degradation of Sp1 Promotes Cellular Senescence.” GeroScience 44 (2): 683–698. http://dx.doi.org/10.1007/s11357-021-00456-5.
  • Tahara, M., Y. Fujino, K. Yamasaki, K. Oda, T. Kido, N. Sakamoto, T. Kawanami, K. Kataoka, et al. 2021. “Exposure to PM2.5 is a Risk Factor for Acute Exacerbation of Surgically Diagnosed Idiopathic Pulmonary Fibrosis: A Case-Control Study.” Respiratory Research 22 (1): 80. http://dx.doi.org/10.1186/s12931-021-01671-6
  • Terradas, M., M. Martin, and A. Genesca. 2016. “Impaired Nuclear Functions in Micronuclei Results in Genome Instability and Chromothripsis.” Archives of Toxicology 90 (11): 2657–2667. http://dx.doi.org/10.1007/s00204-016-1818-4.
  • Van Deursen, J. M. 2014. “The Role of Senescent Cells in Ageing.” Nature 509 (7501): 439–446. http://dx.doi.org/10.1038/nature13193.
  • Vincent, J., C. Adura, P. Gao, A. Luz, L. Lama, Y. Asano, R. Okamoto, T. Imaeda, et al. 2017. “Small Molecule Inhibition of cGAS Reduces Interferon Expression in Primary Macrophages from Autoimmune Mice.” Nature Communications 8 (1): 750. http://dx.doi.org/10.1038/s41467-017-00833-9
  • Wang, C., Z. Y. Sun, C. X. Zhao, Z. W. Zhang, H. R. Wang, Y. Liu, Y. F. Guo, B. T. Zhang, et al. 2021. “Maintaining Manganese in Tumor to Activate cGAS-STING Pathway Evokes a Robust Abscopal anti-Tumor Effect.” Journal of Controlled Release: Official Journal of the Controlled Release Society 331: 480–490. http://dx.doi.org/10.1016/j.jconrel.2021.01.036.
  • Wang, W. J., X. M. Chen, and G. Y. Cai. 2021. “Cellular Senescence and the Senescence-Associated Secretory Phenotype: Potential Therapeutic Targets for Renal Fibrosis.” Experimental Gerontology 151: 111403. http://dx.doi.org/10.1016/j.exger.2021.111403.
  • Wang, Z., L. M. Ma, M. Q. Su, Y. R. Zhou, K. Mao, C. Q. Li, G. Y. Peng, et al. 2018. “Baicalin Induces Cellular Senescence in Human Colon Cancer Cells via Upregulation of DEPP and the Activation of Ras/Raf/MEK/ERK Signaling.” Cell Death & Disease 9: 217. http://dx.doi.org/10.1038/s41419-017-0223-0
  • Wu, B., L. Tang, and M. Kapoor. 2021. “Fibroblasts and Their Responses to Chronic Injury in Pulmonary Fibrosis.” Seminars in Arthritis and Rheumatism 51 (1): 310–317. http://dx.doi.org/10.1016/j.semarthrit.2020.12.003.
  • Yang, H., H. Z. Wang, J. Y. Ren, Q. Chen, and Z. J. J. Chen. 2017. “cGAS is Essential for Cellular Senescence.” Proceedings of the National Academy of Sciences of the United States of America 114 (23): E4612–E4620. http://dx.doi.org/10.1073/pnas.1705499114.
  • Yang, L., C. Li, and X. Tang. 2020. “The Impact of PM2.5 on the Host Defense of Respiratory System.” Frontiers in Cell and Developmental Biology 8: 91. http://dx.doi.org/10.3389/fcell.2020.00091.
  • Zhang, C. Z., A. Spektor, H. Cornils, J. M. Francis, E. K. Jackson, S. W. Liu, M. Meyerson, and D. Pellman. 2015. “Chromothripsis from DNA Damage in Micronuclei.” Nature 522 (7555): 179–184. http://dx.doi.org/10.1038/nature14493.
  • Zhao, J. L., M. Li, Z. H. Wang, J. K. Chen, J. P. Zhao, Y. J. Xu, X. Wei, et al. 2019. “Role of PM2.5 in the Development and Progression of COPD and Its Mechanisms.” Respiratory Research 20 (1): 120. http://dx.doi.org/10.1186/s12931-019-1081-3
  • Zhao, Z., Q. Dong, X. Liu, L. Wei, L. Liu, Y. Li, and X. Wang. 2020. “Dynamic Transcriptome Profiling in DNA Damage-Induced Cellular Senescence and Transient Cell-Cycle Arrest.” Genomics 112 (2): 1309–1317. http://dx.doi.org/10.1016/j.ygeno.2019.07.020.
  • Zhou, Q., J. Chen, J. Zhang, F. Zhou, J. Zhao, X. Wei, K. Zheng, J. Wu, B. Li, and B. Pan. 2022. “Toxicity and Endocrine-Disrupting Potential of PM2.5: Association with Particulate Polycyclic Aromatic Hydrocarbons, Phthalate Esters, and Heavy Metals.” Environmental Pollution (Barking, Essex: 1987) 292 (Pt A): 118349. http://dx.doi.org/10.1016/j.envpol.2021.118349.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.