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Role of PARP1 on DNA damage induced by mineral silicate chrysotile in bronchial epithelial and pleural mesothelial cells

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Abstract

To investigate whether poly (ADP ribose) polymerase-1 (PARP1) is involved in chrysotile-induced DNA damage in pleural mesothelial cells (MeT-5A) and bronchial epithelial cells (BEAS-2B), two PARP1-deficient cell lines were established. Efficiencies of RNA interference on PARP1 were detected by western blot and qPCR. Here, normal cells and PARP1-deficient cells were exposed to chrysotile, and DNA damage and DNA repair were detected by alkaline comet assay. All cells were treated with chrysotile at the indicated concentrations (5, 10, 20, and 40 μg/cm2) for 24 h and then the DNA repair capacity was observed for 12 and 24 h, respectively. The results showed that chrysotile caused DNA damage at an obvious dose-dependent manner in MeT-5A and BEAS-2B cells. In addition, MeT-5A cells had more persistent DNA damage than BEAS-2B. Compared to normal cells, the PARP1-deficient cells were more sensitive to DNA damage caused by chrysotile. In DNA repair experiments, all cell lines recovered from the damage over time. The results of relative repair percentage (RRP) of MeT-5A and BEAS-2B were higher than those of MeT-5A shPARP1 and BEAS-2B shPARP1 cells at all experimental concentrations (except 5 μg/cm2) at 12-h repair. However, RRP of BEAS-2B and BEAS-2B shPARP1 tended to be closer, and RRP of MeT-5A shPARP1 was still lower than that of MeT-5A at 24-h repair. All results suggest that PARP1 plays an important role in early repair of DNA damage in BEAS-2B and MeT-5A cells exposed to chrysotile.

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Data Availability

The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Acencio MM, Soares B, Marchi E, Silva CS, Teixeira LR, Broaddus VC (2015) Inflammatory cytokines contribute to asbestos-induced injury of mesothelial cells. Lung 193:831–837

    Article  CAS  Google Scholar 

  • Boetefuer EL, Lake RJ, Dreval K, Fan HY (2018) Poly(ADP-ribose) polymerase 1 (PARP1) promotes oxidative stress-induced association of Cockayne syndrome group B protein with chromatin. J Biol Chem 293:17863–17874

    Article  CAS  Google Scholar 

  • Cavallo D, Campopiano A, Cardinali G, Casciardi S, De Simone P, Kovacs D, Perniconi B, Spagnoli G, Ursini CL, Fanizza C (2004) Cytotoxic and oxidative effects induced by man-made vitreous fibers (MMVFs) in a human mesothelial cell line. Toxicology 201:219–229

    Article  CAS  Google Scholar 

  • Courtice MN, Lin S, Wang X (2012) An updated review on asbestos and related diseases in China. Int J Occup Environ Health 18:247–253

    Article  CAS  Google Scholar 

  • Cui Y, Ma J, Ye W, Han Z, Dong F, Deng J, Zhang Q (2018a) Chrysotile and rock wool fibers induce chromosome aberrations and DNA damage in V79 lung fibroblast cells. Environ Sci Pollut Res Int 25:22328–22333

    Article  CAS  Google Scholar 

  • Cui Y, Wang Y, Deng J, Hu G, Dong F, Zhang Q (2018b) Chrysotile effects on the expression of anti-oncogene P53 and P16 and oncogene C-jun and C-fos in Wistar rats' lung tissues. Environ Sci Pollut Res Int 25:22378–22388

    Article  CAS  Google Scholar 

  • Cui Y, Zha Y, Li T, Bai J, Tang L, Deng J, He R, Dong F, Zhang Q (2019) Oxidative effects of lungs in Wistar rats caused by long-term exposure to four kinds of China representative chrysotile. Environ Sci Pollut Res Int 26:18708–18718

    Article  CAS  Google Scholar 

  • Dhakal K, Gadupudi GS, Lehmler H-J, Ludewig G, Duffel MW, Robertson LW (2018) Sources and toxicities of phenolic polychlorinated biphenyls (OH-PCBs). Environ Sci Pollut Res Int 25(17):16277–16290

  • Donaldson K, Oberdörster G (2011) Continued controversy on chrysotile biopersistence. Int J Occup Environ Health 17:98–99

    Article  Google Scholar 

  • Feder IS, Tischoff I, Theile A, Schmitz I, Merget R, Tannapfel A (2017) The asbestos fibre burden in human lungs: new insights into the chrysotile debate. Eur Respir J 49. https://doi.org/10.1183/13993003.02534-2016

  • Gilham C (2018) Past and current asbestos exposure and future mesothelioma risks in Britain: the Inhaled Particles Study (TIPS). Int J Epidemiol 47:1745–1756

    Article  Google Scholar 

  • Hiraku Y, Sakai K, Shibata E, Kamijima M, Hisanaga N, Ma N, Kawanishi S, Murata M (2014) Formation of the nitrative DNA lesion 8-nitroguanine is associated with asbestos contents in human lung tissues: a pilot study. J Occup Health 56:186–196

    Article  CAS  Google Scholar 

  • Huo T, Dong F, Deng J, Zhang Q, Ye W, Zhang W, Wang P, Sun D (2018) In vitro genotoxicity of asbestos substitutes induced by coupled stimulation of dissolved high-valence ions and oxide radicals. Environ Sci Pollut Res Int 25:22356–22367

    Article  CAS  Google Scholar 

  • Kim SJ, Cheresh P, Jablonski RP, Morales-Nebreda L, Cheng Y, Hogan E, Yeldandi A, Chi M, Piseaux R, Ridge K, Michael Hart C, Chandel N, Scott Budinger GR, Kamp DW (2016) Mitochondrial catalase overexpressed transgenic mice are protected against lung fibrosis in part via preventing alveolar epithelial cell mitochondrial DNA damage. Free Radic Biol Med 101:482–490

    Article  CAS  Google Scholar 

  • Li P, Liu T, Kamp DW, Lin Z, Wang Y, Li D, Yang L, He H, Liu G (2015) The c-Jun N-terminal kinase signaling pathway mediates chrysotile asbestos-induced alveolar epithelial cell apoptosis. Mol Med Rep 11:3626–3634

    Article  CAS  Google Scholar 

  • Lindberg HK, Falck GC, Singh R, Suhonen S, Järventaus H, Vanhala E, Catalán J, Farmer PB, Savolainen KM, Norppa H (2013) Genotoxicity of short single-wall and multi-wall carbon nanotubes in human bronchial epithelial and mesothelial cells in vitro. Toxicology 313:24–37

    Article  CAS  Google Scholar 

  • Loomis D, Richardson DB, Elliott L (2019) Quantitative relationships of exposure to chrysotile asbestos and mesothelioma mortality. Am J Ind Med 62:471–477

    Article  CAS  Google Scholar 

  • Pinton G, Manente AG, Murer B, De Marino E, Mutti L, Moro L (2013) PARP1 inhibition affects pleural mesothelioma cell viability and uncouples AKT/mTOR axis via SIRT1. J Cell Mol Med 17:233–241

    Article  Google Scholar 

  • Rai B, Mercurio SD (2020) Environmentally relevant exposures of male mice to carbendazim and thiram cause persistent genotoxicity in male mice. Environ Sci Pollut Res Int 27(10):10629–10641

  • Rissel D, Peiter E (2019) Poly(ADP-ribose) polymerases in plants and their human counterparts: parallels and peculiarities. Int J Mol Sci 20. https://doi.org/10.3390/ijms20071638

  • Spivak G (2015) Nucleotide excision repair in humans. DNA Repair (Amst) 36:13–18

    Article  CAS  Google Scholar 

  • Tomasetti M, Amati M, Nocchi L, Saccucci F, Strafella E, Staffolani S, Tarquini LM, Carbonari D, Alleva R, Borghi B, Neuzil J, Bracci M, Santarelli L (2011) Asbestos exposure affects poly(ADP-ribose) polymerase-1 activity: role in asbestos-induced carcinogenesis. Mutagenesis 26:585–591

    Article  CAS  Google Scholar 

  • Turci F, Colonna M, Tomatis M, Mantegna S, Cravotto G, Gulino G, Aldieri E, Ghigo D, Fubini B (2012) Surface reactivity and cell responses to chrysotile asbestos nanofibers. Chem Res Toxicol 25:884–894

    Article  CAS  Google Scholar 

  • Westphal GA, Rosenkranz N, Brik A, Weber D, Föhring I, Monsé C, Kaiser N, Hellack B, Mattenklott M, Brüning T, Johnen G, Bünger J (2019) Multi-walled carbon nanotubes induce stronger migration of inflammatory cells in vitro than asbestos or granular particles but a similar pattern of inflammatory mediators. Toxicol in Vitro 58:215–223

    Article  CAS  Google Scholar 

  • Xia W, Ci S, Li M, Wang M, Dianov GL, Ma Z, Li L, Hua K, Alagamuthu K-K, Qing L, Luo L, Edick AM, Liu L, Hu Z, He L, Pan F, Guo Z (2019) Two-way crosstalk between BER and c-NHEJ repair pathway is mediated by Pol-β and Ku70. FASEB J 33:11668–11681

    Article  CAS  Google Scholar 

  • Zanetti TA, Biaz BI, Coatti GC, Baranoski A, Marques LA, Corveloni AC, Mantovani MS (2019) Mitotic spindle defects and DNA damage induced by dimethoxycurcumin lead to an intrinsic apoptosis pathway in HepG2/C3A cells. Toxicol in Vitro 61:104643

    Article  CAS  Google Scholar 

  • Zhang M, Chen J, Jiang Z, Zhu L, Wu W, Xiao Y, Chen K (2017) Chrysotile causes human bronchial epithelial cell apoptosis in response to the fas-mediated apoptosis pathway. Pathobiology 84:229–236

    Article  Google Scholar 

  • Zhang M, Xia H, Yu M, Zhu L, Ju L, Chen J, Zhao J, Xiao Y, Chen K (2018) N-acetylcysteine prevents cytotoxic effects induced by man-made mineral fibers in a human bronchial epithelial cell line. Toxicol in Vitro 53:200–207

    Article  CAS  Google Scholar 

  • Zhu L, Ju L, Xiao Y, Zhang M, Zhong H, Zhang X (2011) Malignant transformation and differential expression of mismatch repair genes induced by chrysotile. Chin Occup Med 38:218–219 (in Chinese)

    Google Scholar 

Download references

Funding

This work was funded by Health and Family Planning Commission of Zhejiang Province (2021KY131, 2018KY343. 2017ZD014, and 2019KY360), Special Project of Hangzhou Medical College (YS2021013) and Natural Science Foundation of Zhejiang Province (LQY18H260001).

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Author notes

  1. Min Zhang and Hailin Xia contributed equally to this study and should be considered co-first authors.

Authors and Affiliations

  1. Hangzhou Medical College, Tianmushan Road 182, Zhejiang, 310007, Hangzhou, China

    Min Zhang, Hailin Xia, Min Yu, Li Ju, Yun Xiao & Lijin Zhu

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  1. Min Zhang
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  2. Hailin Xia
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  3. Min Yu
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  4. Li Ju
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Contributions

Material preparation, data collection, and analysis were performed by Min Zhang, Hailin Xia, and Lijin Zhu. The first draft of the manuscript was written by Min Zhang and Hailin Xia, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Min Zhang, Hailin Xia, and Lijin Zhu: Conceptualization; Min Zhang, Hailin Xia, and Min Yu: Methodology; Yun Xiao, Lijin Zhu, and Li Ju: Formal analysis and investigation; Min Zhang and Hailin Xia: Writing - original draft preparation; Lijin Zhu, Min Zhang, andYun Xiao: Writing - review and editing; Lijin Zhu, Hailin Xia, andYun Xiao: Funding acquisition; Lijin Zhu: Resources; Min Yu: Supervision.

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Correspondence to Lijin Zhu.

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Zhang, M., Xia, H., Yu, M. et al. Role of PARP1 on DNA damage induced by mineral silicate chrysotile in bronchial epithelial and pleural mesothelial cells. Environ Sci Pollut Res 28, 40871–40878 (2021). https://doi.org/10.1007/s11356-021-13464-x

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