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Benzo[a]pyrene osteotoxicity and the regulatory roles of genetic and epigenetic factors: A review

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Pages 3244-3282 | Published online: 05 May 2021

References

  • Abdel-Shafy, H. I., & Mansour, M. S. (2016). A review on polycyclic aromatic hydrocarbons: Source, environmental impact, effect on human health and remediation. Egyptian Journal of Petroleum, 25(1), 107–123.
  • Al-Bashaireh, A. M., Haddad, L. G., Weaver, M., Chengguo, X., Kelly, D. L., & Yoon, S. (2018). The effect of tobacco smoking on bone mass: An overview of pathophysiologic mechanisms. Journal of Osteoporosis, 2018. https://doi.org/https://doi.org/10.1155/2018/1206235
  • Alhaji, U. N., Larsen, M. C., Bushkofsky, J. R., Czuprynski, C. J., & Jefcoate, C. R. (2011). Acute disruption of bone marrow hematopoiesis by benzo[a]pyrene is selectively reversed by aryl hydrocarbon receptor-mediated processes. Molecular Pharmacology, 79(4), 724–734.
  • An, L., Shi, Q., Fan, M., Huang, G., Zhu, M., Zhang, M., Liu, Y., & Weng, Y. (2020). Benzo[a]pyrene injures BMP2-induced osteogenic differentiation of mesenchymal stem cells through AhR reducing BMPRII. Ecotoxicology and Environmental Safety, 203, 110930.
  • Anderson, J. D., Lowary, P. T., & Widom, J. (2001). Effects of histone acetylation on the equilibrium accessibility of nucleosomal DNA target sites. Journal of Molecular Biology, 307(4), 977–985.
  • Baek, W. Y., & Kim, J. E. (2011). Transcriptional regulation of bone formation. Frontiers in Bioscience (Scholar Edition), 3, 126.
  • Baglìo, S. R., Devescovi, V., Granchi, D., & Baldini, N. (2013). MicroRNA expression profiling of human bone marrow mesenchymal stem cells during osteogenic differentiation reveals Osterix regulation by miR-31. Gene, 527(1), 321–331.
  • Bak, Y., Jang, H. J., Seo, J. H., No, S. H., Chae, J. I., Hong, J., & Yoon, D. Y. (2018). Benzo[a]pyrene alters the expression of genes in A549 lung cancer cells and cancer stem cells. Journal of Microbiology & Biotechnology, 28(3), 425–431.
  • Bártová, E., Krejčí, J., Harničarová, A., Galiová, G., & Kozubek, S. (2008). Histone modifications and nuclear architecture: A review. Journal of Histochemistry & Cytochemistry, 56(8), 711–721.
  • Bellavia, D., De Luca, A., Carina, V., Costa, V., Raimondi, L., Salamanna, F., Alessandro, R., Fini, M., & Giavaresi, G. (2019). Deregulated miRNAs in bone health: Epigenetic roles in osteoporosis. Bone, 122, 52–75. https://doi.org/https://doi.org/10.1016/j.bone.2019.02.013
  • Bi, X., Slater, D. M., Ohmori, H., & Vaziri, C. (2005). DNA polymerase κ is specifically required for recovery from the benzo[a]pyrene-dihydrodiol epoxide (BPDE)-induced S-phase checkpoint. Journal of Biological Chemistry, 280(23), 22343–22355.
  • Blomen, V. A., & Boonstra, J. (2011). Stable transmission of reversible modifications: Maintenance of epigenetic information through the cell cycle. Cellular & Molecular Life Sciences, 68(1), 27–44.
  • Boer, J. D., Licht, R., Bongers, M., Klundert, T. V. D., Arends, R., & Blitterswijk, C. V. (2006). Inhibition of histone acetylation as a tool in bone tissue engineering. Tissue Engineering, 12(10), 2927–2937.
  • Borgen, A., Darvey, H., Castagnoli, N., Crocker, T. T., Rasmussen, R. E., & Wang, I. Y. (1973). Metabolic conversion of benzo[a]pyrene by Syrian hamster liver microsomes and binding of metabolites to deoxyribonucleic acid. Journal of Medicinal Chemistry, 16(5), 502–506.
  • Boström, C. E., Gerde, P., Hanberg, A., Jernström, B., Johansson, C., Kyrklund, T., Rannug, A., Törnqvist, M., Victorin, K., & Westerholm, R. (2002). Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environmental Health Perspectives, 110(suppl 3), 451–488.
  • Boyle, W. J., Simonet, W. S., & Lacey, D. L. (2003). Osteoclast differentiation and activation. Nature, 423(6937), 337–342.
  • Boysen, G., & Hecht, S. S. (2003). Analysis of DNA and protein adducts of benzo[a]pyrene in human tissues using structure-specific methods. Mutation Research/Reviews in Mutation Research, 543(1), 17–30.
  • Brevik, A., Lindeman, B., Brunborg, G., & Duale, N. (2012). Paternal benzo[a]pyrene exposure modulates microRNA expression patterns in the developing mouse embryo. International Journal of Cell Biology, 2012, 407431. https://doi.org/https://doi.org/10.1155/2012/407431
  • Brevik, A., Lindeman, B., Rusnakova, V., Olsen, A. K., Brunborg, G., & Duale, N. (2012). Paternal benzo[a]pyrene exposure affects gene expression in the early developing mouse embryo. Toxicological Sciences, 129(1), 157–165. https://doi.org/https://doi.org/10.1093/toxsci/kfs187
  • Brookes, P., & Lawley, P. D. (1964). Evidence for the binding of polynuclear aromatic hydrocarbons to the nucleic acids of mouse skin: Relation between carcinogenic power of hydrocarbons and their binding to deoxyribonucleic acid. Nature, 202(4934), 781–784.
  • Cai, L., Li, J., Yu, L., Wei, Y., Miao, Z., Chen, M., & Huang, R. (2019). Characterization of transcriptional responses mediated by benzo[a]pyrene stress in a new marine fish model of goby, Mugilogobius chulae. Genes & Genomics, 41(1), 113–123. https://doi.org/https://doi.org/10.1007/s13258-018-0743-8
  • Caiment, F., Gaj, S., Claessen, S., & Kleinjans, J. (2015). High-throughput data integration of RNA–miRNA–circRNA reveals novel insights into mechanisms of benzo[a]pyrene-induced carcinogenicity. Nucleic Acids Research, 43(5), 2525–2534.
  • Chappell, G., Pogribny, I. P., Guyton, K. Z., & Rusyn, I. (2016). Epigenetic alterations induced by genotoxic occupational and environmental human chemical carcinogens: A systematic literature review. Mutation Research/Reviews in Mutation Research, 768, 27–45.
  • Chen, C., Cheng, P., Xie, H., Zhou, H. D., Wu, X. P., Liao, E. Y., & Luo, X. H. (2014). MiR‐503 regulates osteoclastogenesis via targeting RANK. Journal of Bone & Mineral Research, 29(2), 338–347.
  • Chen, Y., Wang, X., Yang, M., Ruan, W., Wei, W., Gu, D., Wang, J., Guo, X., Guo, L., & Yuan, Y. (2018). miR-145-5p increases osteoclast numbers in vitro and aggravates bone erosion in collagen-induced arthritis by targeting osteoprotegerin. Medical Science Monitor: International Medical Journal of Experimental & Clinical Research, 24, 5292.
  • Chen, Y. H., Yeh, F. L., Yeh, S. P., Ma, H. T., Hung, S. C., Hung, M. C., & Li, L. Y. (2011). Myocyte enhancer factor-2 interacting transcriptional repressor (MITR) is a switch that promotes osteogenesis and inhibits adipogenesis of mesenchymal stem cells by inactivating peroxisome proliferator-activated receptor γ-2. Journal of Biological Chemistry, 286(12), 10671–10680. https://doi.org/https://doi.org/10.1074/jbc.M110.199612
  • Chen, Z., & Zhang, Y. (2020). Role of mammalian DNA methyltransferases in development. Annual Review of Biochemistry, 89, 135–158.
  • Cheng, P., Chen, C., He, H. B., Hu, R., Zhou, H. D., Xie, H., Zhu, W., Dai, R. C., Wu, X. P., Liao, E. Y., & Luo, X. H. (2013). miR‐148a regulates osteoclastogenesis by targeting V‐maf musculoaponeurotic fibrosarcoma oncogene homolog B. Journal of Bone & Mineral Research, 28(5), 1180–1190.
  • Chepelev, N. L., Moffat, I. D., Bowers, W. J., & Yauk, C. L. (2015). Neurotoxicity may be an overlooked consequence of benzo[a]pyrene exposure that is relevant to human health risk assessment. Mutation Research/Reviews in Mutation Research, 764, 64–89.
  • Chiba, N., Furukawa, K. I., Takayama, S., Asari, T., Chin, S., Harada, Y., Kumagai, G., Wada, K., Tanaka, T., Ono, A., Motomura, S., Murakami, M., & Ishibashi, Y. (2015). Decreased DNA methylation in the promoter region of the WNT5A and GDNF genes may promote the osteogenicity of mesenchymal stem cells from patients with ossified spinal ligaments. Journal of Pharmacological Sciences, 127(4), 467–473.
  • Cho, H. H., Park, H. T., Kim, Y. J., Bae, Y. C., Suh, K. T., & Jung, J. S. (2005). Induction of osteogenic differentiation of human mesenchymal stem cells by histone deacetylase inhibitors. Journal of Cellular Biochemistry, 96(3), 533–542.
  • Colli-Dula, R. C., Fang, X., Moraga-Amador, D., Albornoz-Abud, N., Zamora-Bustillos, R., Conesa, A., Zapata-Perez, O., Moreno, D., & Hernandez-Nuñez, E. (2018). Transcriptome analysis reveals novel insights into the response of low-dose benzo[a]pyrene exposure in male tilapia. Aquatic Toxicology, 201, 162–173.
  • Cong, F., Wu, N., Tian, X., Fan, J., Liu, J., Song, T., & Fu, H. (2017). MicroRNA-34c promotes osteoclast differentiation through targeting LGR4. Gene, 610, 1–8.
  • Cook, J. W., Hewett, C. L., & Hieger, I. (1933). 106. The isolation of a cancer-producing hydrocarbon from coal tar. Parts I, II, and III. Journal of the Chemical Society (Resumed), 395. https://doi.org/https://doi.org/10.1039/jr9330000395
  • Corrales, J., Fang, X., Thornton, C., Mei, W., Barbazuk, W. B., Duke, M., Scheffler, B. E., & Willett, K. L. (2014). Effects on specific promoter DNA methylation in zebrafish embryos and larvae following benzo[a]pyrene exposure. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 163, 37–46. https://doi.org/https://doi.org/10.1016/j.cbpc.2014.02.005
  • Corrales, J., Thornton, C., White, M., & Willett, K. L. (2014). Multigenerational effects of benzo[a]pyrene exposure on survival and developmental deformities in zebrafish larvae. Aquatic Toxicology, 148, 16–26. https://doi.org/https://doi.org/10.1016/j.aquatox.2013.12.028
  • Crockett, J. C., Rogers, M. J., Coxon, F. P., Hocking, L. J., & Helfrich, M. H. (2011). Bone remodelling at a glance. Journal of Cell Science, 124(7), 991–998.
  • de la Rica, L., García-Gómez, A., Comet, N. R., Rodríguez-Ubreva, J., Vento-Tormo, R., Álvarez-Errico, D., García, M., Gómez-Vaquero, C., & Ballestar, E. (2015). NF-κB-direct activation of microRNAs with repressive effects on monocyte-specific genes is critical for osteoclast differentiation. Genome Biology, 16(1), 2.
  • Delgado-Calle, J., Sañudo, C., Fernández, A. F., García-Renedo, R., Fraga, M. F., & Riancho, J. A. (2012). Role of DNA methylation in the regulation of the RANKL-OPG system in human bone. Epigenetics, 7(1), 83–91.
  • Deng, L., Liu, H., & Deng, Q. (2021). Physiologically-based pharmacokinetic modeling of benzo[a]pyrene and the metabolite in humans of different ages. International Journal of Environmental Health Research, 31(2), 202–214. https://doi.org/https://doi.org/10.1080/09603123.2019.1640355
  • Denissenko, M. F., Pao, A., Tang, M. S., & Pfeifer, G. P. (1996). Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science, 274(5286), 430–432.
  • DiGirolamo, D. J., Clemens, T. L., & Kousteni, S. (2012). The skeleton as an endocrine organ. Nature Reviews Rheumatology, 8(11), 674.
  • Dou, C., Zhang, C., Kang, F., Yang, X., Jiang, H., Bai, Y., Xiang, J., Xu, J., & Dong, S. (2014). MiR-7b directly targets DC-STAMP causing suppression of NFATc1 and c-Fos signaling during osteoclast fusion and differentiation. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1839(11), 1084–1096. https://doi.org/https://doi.org/10.1016/j.bbagrm.2014.08.002
  • Duan, H., Jiang, Y., Zhang, H., & Wu, Y. (2010). MiR-320 and miR-494 affect cell cycles of primary murine bronchial epithelial cells exposed to benzo[a]pyrene. Toxicology in Vitro, 24(3), 928–935.
  • Dudakovic, A., Camilleri, E. T., Xu, F., Riester, S. M., McGee-Lawrence, M. E., Bradley, E. W., Paradise, C. R., Lewallen, E. A., Thaler, R., Deyle, D. R., Larson, A. N., Lewallen, D. G., Dietz, A. B., Stein, G. S., Montecino, M. A., Westendorf, J. J., & van Wijnen, A. J. (2015). Epigenetic control of skeletal development by the histone methyltransferase Ezh2. Journal of Biological Chemistry, 290(46), 27604–27617.
  • Fang, X., Corrales, J., Thornton, C., Clerk, T., Scheffler, B. E., & Willett, K. L. (2015). Transcriptomic changes in zebrafish embryos and larvae following benzo[a]pyrene exposure. Toxicological Sciences, 146(2), 395–411.
  • Fang, X., Thornton, C., Scheffler, B. E., & Willett, K. L. (2013). Benzo[a]pyrene decreases global and gene specific DNA methylation during zebrafish development. Environmental Toxicology & Pharmacology, 36(1), 40–50.
  • Feng, Y., Zhou, A., Zhang, Y., Liu, S., Pan, Z., Zou, J., & Xie, S. (2020). Transcriptomic changes in western mosquitofish (Gambusia affinis) liver following benzo[a]pyrene exposure. Environmental Science and Pollution Research, 27(17), 21924–21938.
  • Fernández, I., Gavaia, P. J., Laizé, V., & Cancela, M. L. (2018). Fish as a model to assess chemical toxicity in bone. Aquatic Toxicology, 194, 208–226.
  • Filippakopoulos, P., & Knapp, S. (2014). Targeting bromodomains: Epigenetic readers of lysine acetylation. Nature Reviews Drug Discovery, 13(5), 337–356.
  • Filippakopoulos, P., Picaud, S., Mangos, M., Keates, T., Lambert, J. P., Barsyte-Lovejoy, D., Felletar, I., Volkmer, R., Müller, S., Pawson, T., Gingras, A. C., Arrowsmith, C. H., & Knapp, S. (2012). Histone recognition and large-scale structural analysis of the human bromodomain family. Cell, 149(1), 214–231.
  • Franceschetti, T., Kessler, C. B., Lee, S. K., & Delany, A. M. (2013). miR-29 promotes murine osteoclastogenesis by regulating osteoclast commitment and migration. Journal of Biological Chemistry, 288(46), 33347–33360.
  • Fu, I., Cai, Y., Geacintov, N. E., Zhang, Y., & Broyde, S. (2017). Nucleosome histone tail conformation and dynamics: Impacts of lysine acetylation and a nearby minor groove benzo[a]pyrene-derived lesion. Biochemistry, 56(14), 1963–1973. https://doi.org/https://doi.org/10.1021/acs.biochem.6b01208
  • Gámez, B., Rodriguez-Carballo, E., & Ventura, F. (2014). MicroRNAs and post-transcriptional regulation of skeletal development. Journal of Molecular Endocrinology, 52(3), R179–R197.
  • Gao, D., Lin, J., Ou, K., Chen, Y., Li, H., Dai, Q., Yu, Z., & Wang, C. (2018). Embryonic exposure to benzo[a]pyrene inhibits reproductive capability in adult female zebrafish and correlation with DNA methylation. Environmental Pollution, 240, 403–411.
  • Gelboin, H. V. (1980). Benzo[a]pyrene metabolism, activation and carcinogenesis: Role and regulation of mixed-function oxidases and related enzymes. Physiological Reviews, 60(4), 1107–1166. https://doi.org/https://doi.org/10.1152/physrev.1980.60.4.1107
  • Ghayor, C., & Weber, F. E. (2016). Epigenetic regulation of bone remodeling and its impacts in osteoporosis. International Journal of Molecular Sciences, 17(9), 1446.
  • Grover, P. L., & Sims, P. (1986). Biochemical Journal, 110, 159–160.
  • Guo, H., Zhu, P., Yan, L., Li, R., Hu, B., Lian, Y., & Jin, X. (2014). The DNA methylation landscape of human early embryos. Nature, 511(7511), 606–610.
  • Guo, J. U., Su, Y., Zhong, C., Ming, G. L., & Song, H. (2011). Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond. Cell Cycle, 10(16), 2662–2668.
  • Ha, M., & Kim, V. N. (2014). Regulation of microRNA biogenesis. Nature Reviews Molecular Cell Biology, 15(8), 509–524.
  • Haddow, A. (1935). Influence of certain polycyclic hydrocarbons on the growth of the Jensen rat sarcoma. Nature, 136(3448), 868–869.
  • Hadjidakis, D. J., & Androulakis, I. I. (2006). Bone remodeling. Annals of the New York Academy of Sciences, 1092(1), 385–396.
  • Hahn, M. E. (2002). Aryl hydrocarbon receptors: Diversity and evolution. Chemico-Biological Interactions, 141(1-2), 131–160. https://doi.org/https://doi.org/10.1016/S0009-2797(02)00070-4
  • Halappanavar, S., Wu, D., Williams, A., Kuo, B., Godschalk, R. W., Van Schooten, F. J., & Yauk, C. L. (2011). Pulmonary gene and microRNA expression changes in mice exposed to benzo[a]pyrene by oral gavage. Toxicology, 285(3), 133–141.
  • Haritash, A. K., & Kaushik, C. P. (2009). Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): A review. Journal of Hazardous Materials, 169(1-3), 1–15.
  • Hassan, M. Q., Tye, C. E., Stein, G. S., & Lian, J. B. (2015). Non-coding RNAs: Epigenetic regulators of bone development and homeostasis. Bone, 81, 746–756. https://doi.org/https://doi.org/10.1016/j.bone.2015.05.026
  • Hattemer-Frey, H. A., & Travis, C. C. (1991). Benzo[a]pyrene: Environmental partitioning and human exposure. Toxicology & Industrial Health, 7(3), 141–157.
  • He, C., Zuo, Z., Shi, X., Li, R., Chen, D., Huang, X., Chen, Y., & Wang, C. (2011). Effects of benzo[a]pyrene on the skeletal development of Sebastiscus marmoratus embryos and the molecular mechanism involved. Aquatic Toxicology, 101(2), 335–341.
  • Hemming, S., Cakouros, D., Isenmann, S., Cooper, L., Menicanin, D., Zannettino, A., & Gronthos, S. (2014). EZH2 and KDM6A act as an epigenetic switch to regulate mesenchymal stem cell lineage specification. Stem Cells, 32(3), 802–815.
  • Hockley, S. L., Mathijs, K., Staal, Y. C., Brewer, D., Giddings, I., van Delft, J. H., & Phillips, D. H. (2009). Interlaboratory and interplatform comparison of microarray gene expression analysis of HepG2 cells exposed to benzo[a]pyrene. OMICS A Journal of Integrative Biology, 13(2), 115–125.
  • Hornung, M. W., Cook, P. M., Fitzsimmons, P. N., Kuehl, D. W., & Nichols, J. W. (2007). Tissue distribution and metabolism of benzo[a]pyrene in embryonic and larval medaka (Oryzias latipes). Toxicological Sciences, 100(2), 393–405.
  • Hose, J. E., Hannah, J. B., Landolt, M. L., Miller, B. S., Felton, S. P., & Iwaoka, W. T. (1981). Uptake of benzo[α]pyrene by gonadal tissue of flatfish (family Pleuronectidae) and its effects on subsequent egg development. Journal of Toxicology and Environmental Health, Part A Current Issues, 7(6), 991–1000.
  • Hrdlicka, H. C., Lee, S. K., & Delany, A. M. (2019). MicroRNAs are critical regulators of osteoclast differentiation. Current Molecular Biology Reports, 5(1), 65–74.
  • Hu, W., Feng, Z., & Tang, M. S. (2003). Preferential carcinogen − DNA adduct formation at codons 12 and 14 in the human K-ras gene and their possible mechanisms. Biochemistry, 42(33), 10012–10023.
  • Huang, J., Zhao, L., Xing, L., & Chen, D. (2010). MicroRNA‐204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells, 28(2), 357–364.
  • Huang, L., Zuo, Z., Zhang, Y., Wu, M., Lin, J. J., & Wang, C. (2014). Use of toxicogenomics to predict the potential toxic effect of benzo[a]pyrene on zebrafish embryos: Ocular developmental toxicity. Chemosphere, 108, 55–61. https://doi.org/https://doi.org/10.1016/j.chemosphere.2014.02.078
  • Husain, A., & Jeffries, M. A. (2017). Epigenetics and bone remodeling. Current Osteoporosis Reports, 15(5), 450–458.
  • Inose, H., Ochi, H., Kimura, A., Fujita, K., Xu, R., Sato, S., Iwasaki, M., Sunamura, S., Takeuchi, Y., Fukumoto, S., Saito, K., Nakamura, T., Siomi, H., Ito, H., Arai, Y., Shinomiya, K., & Takeda, S. (2009). A microRNA regulatory mechanism of osteoblast differentiation. Proceedings of the National Academy of Sciences, 106(49), 20794–20799.
  • International Agency for Research on Cancer (IARC). (2010). Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures (Vol. 92). IARC Press, International Agency for Research on Cancer.
  • IARC. 2012. Monographs on the evaluation of carcinogenic risks to humans. http://monographs.iarc.fr/ENG/Classification/
  • Iqbal, J., Sun, L., Cao, J., Yuen, T., Lu, P., Bab, I., Leu, N. A., Srinivasan, S., Wagage, S., Hunter, C. A., Nebert, D. W., Zaidi, M., & Avadhani, N. G. (2013). Smoke carcinogens cause bone loss through the aryl hydrocarbon receptor and induction of Cyp1 enzymes. Proceedings of the National Academy of Sciences, 110(27), 11115–11120.
  • James, M. O., Tong, Z., Rowland-Faux, L., Venugopal, C. S., & Kleinow, K. M. (2001). Intestinal bioavailability and biotransformation of 3-hydroxybenzo[a]pyrene in an isolated perfused preparation from channel catfish, Ictalurus punctatus. Drug Metabolism and Disposition, 29(5), 721–728.
  • Jeong, S. I., Lee, S. E., Yang, H., Park, C. S., Cho, J. J., & Park, Y. S. (2012). MicroRNA microarray analysis of human umbilical vein endothelial cells exposed to benzo[a]pyrene. BioChip Journal, 6(2), 191–196.
  • Jia, J., Tian, Q., Ling, S., Liu, Y., Yang, S., & Shao, Z. (2013). miR‐145 suppresses osteogenic differentiation by targeting Sp7. FEBS Letters, 587(18), 3027–3031.
  • Jiang, H., Gelhaus, S. L., Mangal, D., Harvey, R. G., Blair, I. A., & Penning, T. M. (2007). Metabolism of benzo[a]pyrene in human bronchoalveolar H358 cells using liquid chromatography–mass spectrometry. Chemical Research in Toxicology, 20(9), 1331–1341.
  • Jiang, X., Wu, X., Chen, F., He, W., Chen, X., Liu, L., & Tang, H. (2018). The profiles and networks of miRNA, lncRNA, mRNA, and circRNA in benzo[a]pyrene-transformed bronchial epithelial cells. The Journal of Toxicological Sciences, 43(4), 281–289.
  • Jing, D., Hao, J., Shen, Y., Tang, G., Li, M. L., Huang, S. H., & Zhao, Z. H. (2015). The role of microRNAs in bone remodeling. International Journal of Oral Science, 7(3), 131–143.
  • Juhasz, A. L., & Naidu, R. (2000). Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: A review of the microbial degradation of benzo[a]pyrene. International Biodeterioration & Biodegradation, 45(1-2), 57–88.
  • Kang, M. I., Kim, H. S., Jung, Y. C., Kim, Y. H., Hong, S. J., Kim, M. K., Baek, K. H., Kim, C. C., & Rhyu, M. G. (2007). Transitional CpG methylation between promoters and retroelements of tissue‐specific genes during human mesenchymal cell differentiation. Journal of Cellular Biochemistry, 102(1), 224–239.
  • Kapinas, K., Kessler, C., Ricks, T., Gronowicz, G., & Delany, A. M. (2010). miR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. Journal of Biological Chemistry, 285(33), 25221–25231.
  • Keshava, C., Whipkey, D., & Weston, A. (2005). Transcriptional signatures of environmentally relevant exposures in normal human mammary epithelial cells: Benzo[a]pyrene. Cancer Letters, 221(2), 201–211.
  • Khanal, T., Kim, D., Johnson, A., Choubey, D., & Kim, K. (2015). Deregulation of NR2E3, an orphan nuclear receptor, by benzo[a]pyrene-induced oxidative stress is associated with histone modification status change of the estrogen receptor gene promoter. Toxicology Letters, 237(3), 228–236. https://doi.org/https://doi.org/10.1016/j.toxlet.2015.06.1708
  • Kim, B. M., Rhee, J. S., Jeong, C. B., Lee, S. J., Lee, Y. S., Choi, I. Y., & Lee, J. S. (2014). Effects of benzo[a]pyrene on whole cytochrome P450-involved molecular responses in the marine medaka Oryzias melastigma. Aquatic Toxicology, 152, 232–243.
  • Kim, K. M., & Lim, S. K. (2014). Role of miRNAs in bone and their potential as therapeutic targets. Current Opinion in Pharmacology, 16, 133–141.
  • Kim, Y. J., Bae, S. W., Yu, S. S., Bae, Y. C., & Jung, J. S. (2009). miR‐196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. Journal of Bone & Mineral Research, 24(5), 816–825.
  • Knecht, A. L., Truong, L., Marvel, S. W., Reif, D. M., Garcia, A., Lu, C., Simonich, M. T., & Tanguay, R. L. (2017). Transgenerational inheritance of neurobehavioral and physiological deficits from developmental exposure to benzo[a]pyrene in zebrafish. Toxicology & Applied Pharmacology, 329, 148–157.
  • Kootstra, A., Slaga, T. J., & Olins, D. E. (1979). Interaction of benzo[a]pyrene diol-epoxide with nuclei and isolated chromatin. Chemico-Biological Interactions, 28(2-3), 225–236.
  • Kung, M. H., Yukata, K., O'Keefe, R. J., & Zuscik, M. J. (2012). Aryl hydrocarbon receptor‐mediated impairment of chondrogenesis and fracture healing by cigarette smoke and benzo[a]pyrene. Journal of Cellular Physiology, 227(3), 1062–1070.
  • Labib, S., Guo, C. H., Williams, A., Yauk, C. L., White, P. A., & Halappanavar, S. (2013). Toxicogenomic outcomes predictive of forestomach carcinogenesis following exposure to benzo[a]pyrene: Relevance to human cancer risk. Toxicology & Applied Pharmacology, 273(2), 269–280.
  • Labib, S., Yauk, C., Williams, A., Arlt, V. M., Phillips, D. H., White, P. A., & Halappanavar, S. (2012). Subchronic oral exposure to benzo[a]pyrene leads to distinct transcriptomic changes in the lungs that are related to carcinogenesis. Toxicological Sciences, 129(1), 213–224.
  • Lee, L. L., Lee, J. S. C., Waldman, S. D., Casper, R. F., & Grynpas, M. D. (2002). Polycyclic aromatic hydrocarbons present in cigarette smoke cause bone loss in an ovariectomized rat model. Bone, 30(6), 917–923.
  • Legraverend, C., Guenthner, T. M., & Nebert, D. W. (1984). Importance of the route of administration for genetic differences in benzo[a]pyrene‐induced in utero toxicity and teratogenicity. Teratology, 29(1), 35–47.
  • Lennartsson, A., & Ekwall, K. (2009). Histone modification patterns and epigenetic codes. Biochimica et Biophysica Acta (BBA)-general Subjects, 1790(9), 863–868.
  • Letarouilly, J. G., Broux, O., & Clabaut, A. (2019). New insights into the epigenetics of osteoporosis. Genomics, 111(4), 793–798.
  • Li, E., Zhang, J., Yuan, T., & Ma, B. (2014). MiR-143 suppresses osteogenic differentiation by targeting Osterix. Molecular & Cellular Biochemistry, 390(1-2), 69–74.
  • Li, G., Bu, J., Zhu, Y., Xiao, X., Liang, Z., & Zhang, R. (2015). Curcumin improves bone microarchitecture in glucocorticoid-induced secondary osteoporosis mice through the activation of microRNA-365 via regulating MMP-9. International Journal of Clinical & Experimental Pathology, 8(12), 15684.
  • Li, H., Xie, H., Liu, W., Hu, R., Huang, B., Tan, Y. F., Xu, K., Sheng, Z. F., Zhou, H. D., Wu, X. P., & Luo, X. H. (2009). A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. The Journal of Clinical Investigation, 119(12), 3666–3677.
  • Liang, J., Zhu, H., Li, C., Ding, Y., Zhou, Z., & Wu, Q. (2012). Neonatal exposure to benzo[a]pyrene decreases the levels of serum testosterone and histone H3K14 acetylation of the StAR promoter in the testes of SD rats. Toxicology, 302(2-3), 285–291. https://doi.org/https://doi.org/10.1016/j.tox.2012.08.010
  • Liao, L., Yang, X., Su, X., Hu, C., Zhu, X., Yang, N., Chen, X., Shi, S., Shi, S., & Jin, Y. (2013). Redundant miR-3077-5p and miR-705 mediate the shift of mesenchymal stem cell lineage commitment to adipocyte in osteoporosis bone marrow. Cell Death & Disease, 4(4), e600e600.
  • Liu, C., Xing, X., Chen, L., Li, D., Bai, Q., Wang, Q., & Zhang, Z. (2015). Specific histone modifications regulate the expression of AhR in 16HBE cells exposed to benzo[a]pyrene. Toxicology Research, 4(1), 143–151.
  • Liu, D., Pan, L., Li, Z., Cai, Y., & Miao, J. (2014). Metabolites analysis, metabolic enzyme activities and bioaccumulation in the clam Ruditapes philippinarum exposed to benzo[a]pyrene. Ecotoxicology & Environmental Safety, 107, 251–259.
  • Liu, Q., & Paroo, Z. (2010). Biochemical principles of small RNA pathways. Annual Review of Biochemistry, 79, 295–319.
  • Livingstone, D. R. (1998). The fate of organic xenobiotics in aquatic ecosystems: Quantitative and qualitative differences in biotransformation by invertebrates and fish. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 120(1), 43–49.
  • Lizarraga, D., Gaj, S., Brauers, K. J., Timmermans, L., Kleinjans, J. C., & van Delft, J. H. (2012). Benzo[a]pyrene-induced changes in microRNA–mRNA networks. Chemical Research in Toxicology, 25(4), 838–849.
  • Lozano, C., Duroux-Richard, I., Firat, H., Schordan, E., & Apparailly, F. (2019). MicroRNAs: Key regulators to understand osteoclast differentiation? Frontiers in Immunology, 10, 375–375.
  • Lukashevich, O. V., Baskunov, V. B., Darii, M. V., Kolbanovskiy, A., Baykov, A. A., & Gromova, E. S. (2011). Dnmt3a-CD is less susceptible to bulky benzo[a]pyrene diol epoxide-derived DNA lesions than prokaryotic DNA methyltransferases. Biochemistry, 50(5), 875–881.
  • Ma, Y., Yang, H., & Huang, J. (2018). Icariin ameliorates dexamethasone-induced bone deterioration in an experimental mouse model via activation of microRNA-186 inhibition of cathepsin K. Molecular Medicine Reports, 17(1), 1633–1641.
  • Madeen, E., Siddens, L. K., Uesugi, S., McQuistan, T., Corley, R. A., Smith, J., Waters, K. M., Tilton, S. C., Anderson, K. A., Ognibene, T., Turteltaub, K., & Williams, D. E. (2019). Toxicokinetics of benzo[a]pyrene in humans: Extensive metabolism as determined by UPLC-accelerator mass spectrometry following oral micro-dosing. Toxicology and Applied Pharmacology, 364, 97–105.
  • Malik, A. I., Williams, A., Lemieux, C. L., White, P. A., & Yauk, C. L. (2012). Hepatic mRNA, microRNA, and miR‐34a‐Target responses in mice after 28 days exposure to doses of benzo[a]pyrene that elicit DNA damage and mutation. Environmental and Molecular Mutagenesis, 53(1), 10–21.
  • McGarvey, K. M., Fahrner, J. A., Greene, E., Martens, J., Jenuwein, T., & Baylin, S. B. (2006). Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Research, 66(7), 3541–3549.
  • Mhanni, A. A., & McGowan, R. A. (2004). Global changes in genomic methylation levels during early development of the zebrafish embryo. Development Genes and Evolution, 214(8), 412–417.
  • Miller, E. C. (1951). Studies on the formation of protein-bound derivatives of 3, 4-benzpyrene in the epidermal fraction of mouse skin. Cancer Research, 11(2), 100–108.
  • Mizoguchi, F., Izu, Y., Hayata, T., Hemmi, H., Nakashima, K., Nakamura, T., Kato, S., Miyasaka, N., Ezura, Y., & Noda, M. (2010). Osteoclast‐specific Dicer gene deficiency suppresses osteoclastic bone resorption. Journal of Cellular Biochemistry, 109(5), 866–875.
  • Mizoguchi, F., Murakami, Y., Saito, T., Miyasaka, N., & Kohsaka, H. (2013). miR-31 controls osteoclast formation and bone resorption by targeting RhoA. Arthritis Research & Therapy, 15(5), R102.
  • Mo, J., Au, D. W. T., Wan, M. T., Shi, J., Zhang, G., Winkler, C., Kong, R. Y. C., & Seemann, F. (2020). Multigenerational impacts of benzo[a]pyrene on bone modeling and remodeling in medaka (Oryzias latipes). Environmental Science & Technology, 4(19), 12271–12284.
  • Moffat, I., Chepelev, N. L., Labib, S., Bourdon-Lacombe, J., Kuo, B., Buick, J. K., Lemieux, F., Williams, A., Halappanavar, S., Malik, A., Luijten, M., Aubrecht, J., Hyduke, D. R., Fornace, A. J., Jr., Swartz, C. D., Recio, L., & Yauk, C. L. (2015). Comparison of toxicogenomics and traditional approaches to inform mode of action and points of departure in human health risk assessment of benzo[a]pyrene in drinking water. Critical Reviews in Toxicology, 45(1), 1–43.
  • Mohamed, E. S. A., Song, W. H., Oh, S. A., Park, Y. J., You, Y. A., Lee, S., Choi, J. Y., Kim, Y. J., Jo, I., & Pang, M. G. (2010). The transgenerational impact of benzo[a]pyrene on murine male fertility. Human Reproduction, 25(10), 2427–2433.
  • Monnouchi, S., Maeda, H., Yuda, A., Serita, S., Wada, N., Tomokiyo, A., & Akamine, A. (2016). Benzo[a]pyrene/aryl hydrocarbon receptor signaling inhibits osteoblastic differentiation and collagen synthesis of human periodontal ligament cells. Journal of Periodontal Research, 51(6), 779–788.
  • Monteverdi, G. H., & DiGiulio, R. T. (2000). Oocytic accumulation and tissue distribution of 2, 3, 7, 8‐tetrachlorodibenzo‐p‐dioxin and benzo[a]pyrene in gravid Fundulus heteroclitus. Environmental Toxicology and Chemistry, 19(10), 2512–2518.
  • Musselman, C. A., Lalonde, M. E., Côté, J., & Kutateladze, T. G. (2012). Perceiving the epigenetic landscape through histone readers. Nature Structural & Molecular Biology, 19(12), 1218.
  • Nebert, D. W., Shi, Z., Gálvez-Peralta, M., Uno, S., & Dragin, N. (2013). Oral benzo[a]pyrene: Understanding pharmacokinetics, detoxication, and consequences—Cyp1 knockout mouse lines as a paradigm. Molecular Pharmacology, 84(3), 304–313.
  • Perera, F., Tang, D., Whyatt, R., Lederman, S. A., & Jedrychowski, W. (2005). DNA damage from polycyclic aromatic hydrocarbons measured by benzo[a]pyrene-DNA adducts in mothers and newborns from Northern Manhattan, the World Trade Center Area, Poland, and China. Cancer Epidemiology & Prevention Biomarkers, 14(3), 709–714.
  • Peschansky, V. J., & Wahlestedt, C. (2014). Non-coding RNAs as direct and indirect modulators of epigenetic regulation. Epigenetics, 9(1), 3–12.
  • Phillips, D. H. (1983). Fifty years of benzo[a]pyrene. Nature, 303(5917), 468. https://doi.org/https://doi.org/10.1038/303468a0
  • Pullman, A., & Pullman, B. (1955). Electronic structure and carcinogenic activity of aromatic molecules new developments. Advances in Cancer Research, 3, 117–169.
  • Raggatt, L. J., & Partridge, N. C. (2010). Cellular and molecular mechanisms of bone remodeling. Journal of Biological Chemistry, 285(33), 25103–25108.
  • Rathore, K., & Cekanova, M. (2015). Effects of environmental carcinogen benzo[a]pyrene on canine adipose-derived mesenchymal stem cells. Research in Veterinary Science, 103, 34–43.
  • Reppe, S., Noer, A., Grimholt, R. M., Halldórsson, B. V., Medina‐Gomez, C., Gautvik, V. T., Olstad, O. K., Berg, J. P., Datta, H., Estrada, K., Hofman, A., Uitterlinden, A. G., Rivadeneira, F., Lyle, R., Collas, P., & Gautvik, K. M. (2015). Methylation of bone SOST, its mRNA, and serum sclerostin levels correlate strongly with fracture risk in postmenopausal women. Journal of Bone & Mineral Research, 30(2), 249–256.
  • Rey-Salgueiro, L., Costa, J., Ferreira, M., & Reis-Henriques, M. A. (2011). Evaluation of 3-hydroxy-benzo[a]pyrene levels in Nile tilapia (Oreochromis niloticus) after waterborne exposure to Benzo[a]pyrene. Toxicological & Environmental Chemistry, 93(10), 2040–2054.
  • Rossi, M., Pitari, M. R., Amodio, N., Di Martino, M. T., Conforti, F., Leone, E. C., Paolino, F. M., Del Giudice, T., Iuliano, E., Caraglia, M., Ferrarini, M., Giordano, A., Tagliaferri, P., & Tassone, P. (2013). miR‐29b negatively regulates human osteoclastic cell differentiation and function: Implications for the treatment of multiple myeloma‐related bone disease. Journal of Cellular Physiology, 228(7), 1506–1515.
  • Rust, A. J., Burgess, R. M., Brownawell, B. J., & McElroy, A. E. (2004). Relationship between metabolism and bioaccumulation of benzo[a]pyrene in benthic invertebrates. Environmental Toxicology & Chemistry, 23(11), 2587–2593.
  • Sadikovic, B., Andrews, J., Carter, D., Robinson, J., & Rodenhiser, D. I. (2008). Genome-wide H3K9 histone acetylation profiles are altered in benzopyrene-treated MCF7 breast cancer cells. Journal of Biological Chemistry, 283(7), 4051–4060.
  • Santos, C., de Oliveira, M. T., de Syllos Cólus, I. M., Sofia, S. H., & dos Reis Martinez, C. B. (2018). Expression of cyp1a induced by benzo[a]pyrene and related biochemical and genotoxic biomarkers in the neotropical freshwater fish Prochilodus lineatus. Environmental Toxicology and Pharmacology, 61, 30–37.
  • Schnekenburger, M., Peng, L., & Puga, A. (2007). HDAC1 bound to the Cyp1a1 promoter blocks histone acetylation associated with Ah receptor-mediated trans-activation. Biochimica et Biophysica Acta (BBA)-Gene Structure & Expression, 1769(9-10), 569–578.
  • Seemann, F., Jeong, C. B., Zhang, G., Wan, M. T., Guo, B., Peterson, D. R., Lee, J. S., & Au, D. W. T. (2017). Ancestral benzo[a]pyrene exposure affects bone integrity in F3 adult fish (Oryzias latipes). Aquatic Toxicology, 183, 127–134.
  • Seemann, F., Peterson, D. R., Witten, P. E., Guo, B. S., Shanthanagouda, A. H., Rui, R. Y., Zhang, G., & Au, D. W. (2015). Insight into the transgenerational effect of benzo[a]pyrene on bone formation in a teleost fish (Oryzias latipes). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 178, 60–67.
  • Seisenberger, S., Andrews, S., Krueger, F., Arand, J., Walter, J., Santos, F., Popp, C., Thienpont, B., Dean, W., & Reik, W. (2012). The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Molecular Cell, 48(6), 849–862.
  • Shi, K., Lu, J., Zhao, Y., Wang, L., Li, J., Qi, B., Li, H., & Ma, C. (2013). MicroRNA-214 suppresses osteogenic differentiation of C2C12 myoblast cells by targeting Osterix. Bone, 55(2), 487–494.
  • Shiizaki, K., Kawanishi, M., & Yagi, T. (2017). Modulation of benzo[a]pyrene–DNA adduct formation by CYP1 inducer and inhibitor. Genes and Environment, 39(1), 1–8.
  • Sims, N. A., & Gooi, J. H. (2008). Bone remodeling: Multiple cellular interactions required for coupling of bone formation and resorption. In Seminars in Cell & Developmental Biology, 19(5), 444–451.
  • Sims, P. 1974. Proc. 11th int. Cancer Congr., Florence.
  • Song, Y., Nahrgang, J., & Tollefsen, K. E. (2019). Transcriptomic analysis reveals dose-dependent modes of action of benzo[a]pyrene in polar cod (Boreogadus saida). Science of the Total Environment, 653, 176–189.
  • Souza, T., Jennen, D., van Delft, J., van Herwijnen, M., Kyrtoupolos, S., & Kleinjans, J. (2016). New insights into BaP-induced toxicity: Role of major metabolites in transcriptomics and contribution to hepatocarcinogenesis. Archives of Toxicology, 90(6), 1449–1458.
  • Sparfel, L., Pinel-Marie, M. L., Boize, M., Koscielny, S., Desmots, S., Pery, A., & Fardel, O. (2010). Transcriptional signature of human macrophages exposed to the environmental contaminant benzo[a]pyrene. Toxicological Sciences, 114(2), 247–259.
  • Stadnicka-Michalak, J., Weiss, F. T., Fischer, M., Tanneberger, K., & Schirmer, K. (2018). Biotransformation of benzo[a]pyrene by three rainbow trout (Onchorhynchus mykiss) cell lines and extrapolation to derive a fish bioconcentration factor. Environmental Science & Technology, 52(5), 3091–3100.
  • Sugatani, T., & Hruska, K. A. (2009). Impaired micro-RNA pathways diminish osteoclast differentiation and function. Journal of Biological Chemistry, 284(7), 4667–4678.
  • Sugatani, T., & Hruska, K. A. (2013). Down‐regulation of miR‐21 biogenesis by estrogen action contributes to osteoclastic apoptosis. Journal of Cellular Biochemistry, 114(6), 1217–1222.
  • Sugatani, T., Vacher, J., & Hruska, K. A. (2011). A microRNA expression signature of osteoclastogenesis. Blood, 117(13), 3648–3657.
  • Sun, K. T., Chen, M. Y., Tu, M. G., Wang, I. K., Chang, S. S., & Li, C. Y. (2015). MicroRNA-20a regulates autophagy related protein-ATG16L1 in hypoxia-induced osteoclast differentiation. Bone, 73, 145–153.
  • Svartholm, N. V. 1941. Ark. Kemi Miner. Geol. A15. No.13.
  • Tang, P., Xiong, Q., Ge, W., & Zhang, L. (2014). The role of microRNAs in osteoclasts and osteoporosis. RNA Biology, 11(11), 1355–1363.
  • Tarfiei, G., Noruzinia, M., Soleimani, M., Kaviani, S., Maymand, M. M., Hagh, M. F., & Pujol, P. (2011). ROR2 promoter methylation change in osteoblastic differentiation of mesenchymal stem cells. Cell Journal (Yakhteh), 13(1), 11.
  • Teixeira, C. C., Liu, Y., Thant, L. M., Pang, J., Palmer, G., & Alikhani, M. (2010). Foxo1, a novel regulator of osteoblast differentiation and skeletogenesis. Journal of Biological Chemistry, 285(40), 31055–31065.
  • Teneng, I., Montoya-Durango, D. E., Quertermous, J. L., Lacy, M. E., & Ramos, K. S. (2011). Reactivation of L1 retrotransposon by benzo[a]pyrene involves complex genetic and epigenetic regulation. Epigenetics, 6(3), 355–367. https://doi.org/https://doi.org/10.4161/epi.6.3.14282
  • Teti, A. (2011). Bone development: Overview of bone cells and signaling. Current Osteoporosis Reports, 9(4), 264. https://doi.org/https://doi.org/10.1007/s11914-011-0078-8
  • Tomokiyo, A., Maeda, H., Fujii, S., Monnouchi, S., Wada, N., Hori, K., Koori, K., Yamamoto, N., Teramatsu, Y., & Akamine, A. (2012). Alternation of extracellular matrix remodeling and apoptosis by activation of the aryl hydrocarbon receptor pathway in human periodontal ligament cells. Journal of Cellular Biochemistry, 113(10), 3093–3103.
  • Torvanger, I., Metz, J. R., Olsvik, P. A., Søfteland, L., & Lie, K. K. (2018). Benzo[a]pyrene reduces osteoclast and osteoblast activity in ex‐vivo scales of zebrafish (Danio rerio [Hamilton‐Buchanan, 1822]) and goldfish (Carassius auratus [Linnaeus, 1758]. Journal of Applied Ichthyology, 34(2), 431–439. https://doi.org/https://doi.org/10.1111/jai.13666
  • Tsai, K. S., Yang, R. S., & Liu, S. H. (2004). Benzo[a]pyrene regulates osteoblast proliferation through an estrogen receptor-related cyclooxygenase-2 pathway. Chemical Research in Toxicology, 17(5), 679–684.
  • van Delft, J., Gaj, S., Lienhard, M., Albrecht, M. W., Kirpiy, A., Brauers, K., Claessen, S., Lizarraga, D., Lehrach, H., Herwig, R., & Kleinjans, J. (2012). RNA-Seq provides new insights in the transcriptome responses induced by the carcinogen benzo[a]pyrene. Toxicological Sciences, 130(2), 427–439.
  • Van Kesteren, P. C. E., Zwart, P. E., Schaap, M. M., Pronk, T. E., van Herwijnen, M. H. M., Kleinjans, J. C. S., Bokkers, B. G. H., Godschalk, R. W. L., Zeilmaker, M. J., van Steeg, H., & Luijten, M. (2013). Benzo[a]pyrene-induced transcriptomic responses in primary hepatocytes and in vivo liver: Toxicokinetics is essential for in vivo–in vitro comparisons. Archives of Toxicology, 87(3), 505–515. https://doi.org/https://doi.org/10.1007/s00204-012-0949-5
  • Voronov, I., Heersche, J. N. M., Casper, R. F., Tenenbaum, H. C., & Manolson, M. F. (2005). Inhibition of osteoclast differentiation by polycyclic aryl hydrocarbons is dependent on cell density and RANKL concentration. Biochemical Pharmacology, 70(2), 300–307.
  • Voronov, I., Li, K., Tenenbaum, H. C., & Manolson, M. F. (2008). Benzo[a]pyrene inhibits osteoclastogenesis by affecting RANKL-induced activation of NF-κB. Biochemical Pharmacology, 75(10), 2034–2044.
  • Wang, C., He, H., Wang, L., Jiang, Y., & Xu, Y. (2018). Reduced miR-144-3p expression in serum and bone mediates osteoporosis pathogenesis by targeting RANK. Biochemistry & Cell Biology, 96(5), 627–635.
  • Wang, F. S., Chung, P. C., Lin, C. L., Chen, M. W., Ke, H. J., Chang, Y. H., Chen, Y. S., Wu, S. L., & Ko, J. Y. (2013). MicroRNA‐29a protects against glucocorticoid‐induced bone loss and fragility in rats by orchestrating bone acquisition and resorption. Arthritis & Rheumatism, 65(6), 1530–1540.
  • Wang, J., Li, C. L., Tu, B. J., Yang, K., Mo, T. T., Zhang, R. Y., & Xia, Y. Y. (2018). Integrated epigenetics, transcriptomics, and metabolomics to analyze the mechanisms of benzo[a]pyrene neurotoxicity in the hippocampus. Toxicological Sciences, 166(1), 65–81.
  • Wang, T., Yin, H., Wang, J., Li, Z., Wei, H., Liu, Z. A., Wu, Z., Yan, W., Liu, T., Song, D., Yang, X., Huang, Q., Zhou, W., & Xiao, J. (2015). MicroRNA-106b inhibits osteoclastogenesis and osteolysis by targeting RANKL in giant cell tumor of bone. Oncotarget, 6(22), 18980. https://doi.org/https://doi.org/10.18632/oncotarget.4223
  • Wang, X., & Bhandari, R. K. (2019). DNA methylation dynamics during epigenetic reprogramming of medaka embryo. Epigenetics, 14(6), 611–622.
  • Wang, X., & Bhandari, R. K. (2020a). DNA methylation reprogramming in medaka fish, a promising animal model for environmental epigenetics research. Environmental Epigenetics, 6(1), dvaa008. https://doi.org/https://doi.org/10.1093/eep/dvaa008
  • Wang, X., & Bhandari, R. K. (2020b). The dynamics of DNA methylation during epigenetic reprogramming of primordial germ cells in medaka (Oryzias latipes). Epigenetics, 15(5), 483–498. https://doi.org/https://doi.org/10.1080/15592294.2019.1695341
  • Wang, X., Guo, B., Li, Q., Peng, J., Yang, Z., Wang, A., & Cao, H. (2013). miR-214 targets ATF4 to inhibit bone formation. Nature Medicine, 19(1), 93.
  • Wang, Y., Zhang, J., Li, B., & He, Q. Y. (2019). Advances of proteomics in novel PTM discovery: Applications in cancer therapy. Small Methods, 3(5), 1900041. https://doi.org/https://doi.org/10.1002/smtd.201900041
  • Wei, Y., Chen, Y. H., Li, L. Y., Lang, J., Yeh, S. P., Shi, B., Yang, C. C., Yang, J. Y., Lin, C. Y., Lai, C. C., & Hung, M. C. (2011). CDK1-dependent phosphorylation of EZH2 suppresses methylation of H3K27 and promotes osteogenic differentiation of human mesenchymal stem cells. Nature Cell Biology, 13(1), 87–94.
  • Weisenberger, D. J., & Romano, L. J. (1999). Cytosine methylation in a CpG sequence leads to enhanced reactivity with benzo[a]pyrene diol epoxide that correlates with a conformational change. Journal of Biological Chemistry, 274(34), 23948–23955.
  • Willett, K. L., Gardinali, P. R., Lienesch, L. A., & Di Giulio, R. T. (2000). Comparative metabolism and excretion of benzo[a]pyrene in 2 species of ictalurid catfish. Toxicological Sciences, 58(1), 68–76.
  • Wilson, V. L., & Jones, P. A. (1983). Inhibition of DNA methylation by chemical carcinogens in vitro. Cell, 32(1), 239–246.
  • Witten, P. E., & Huysseune, A. (2009). A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biological Reviews, 84(2), 315–346.
  • Xue, W., & Warshawsky, D. (2005). Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicology & Applied Pharmacology, 206(1), 73–93.
  • Yoon, J. H., Smith, L. E., Feng, Z., Tang, M. S., Lee, C. S., & Pfeifer, G. P. (2001). Methylated CpG dinucleotides are the preferential targets for G-to-T transversion mutations induced by benzo[a]pyrene diol epoxide in mammalian cells: Similarities with the p53 mutation spectrum in smoking-associated lung cancers. Cancer Research, 61(19), 7110–7117.
  • Yu, F. Y., Xie, C. Q., Sun, J. T., Peng, W., & Huang, X. W. (2018). Overexpressed miR-145 inhibits osteoclastogenesis in RANKL-induced bone marrow-derived macrophages and ovariectomized mice by regulation of Smad3. Life Sciences, 202, 11–20.
  • Zhang, J. F., Fu, W. M., He, M. L., Wang, H., Wang, W. M., Yu, S. C., Bian, X. W., Zhou, J., Lin, M. C., Lu, G., Poon, W. S., & Kung, H. F. (2011). MiR-637 maintains the balance between adipocytes and osteoblasts by directly targeting Osterix. Molecular Biology of the Cell, 22(21), 3955–3961.
  • Zhang, N., Lin, C., Huang, X., Kolbanovskiy, A., Hingerty, B. E., Amin, S., Broyde, S., Geacintov, N. E., & Patel, D. J. (2005). Methylation of cytosine at C5 in a CpG sequence context causes a conformational switch of a benzo[a]pyrene diol epoxide-N2-guanine adduct in DNA from a minor groove alignment to intercalation with base displacement. Journal of Molecular Biology, 346(4), 951–965. https://doi.org/https://doi.org/10.1016/j.jmb.2004.12.027
  • Zhang, Q. L., Dong, Z. X., Xiong, Y., Li, H. W., Guo, J., Wang, F., Deng, X. Y., Chen, J. Y., & Lin, L. B. (2019). Genome-wide transcriptional response of microRNAs to the benzo[a]pyrene stress in amphioxus Branchiostoma belcheri. Chemosphere, 218, 205–210.
  • Zhang, W., Tian, F., Zheng, J., Li, S., & Qiang, M. (2016). Chronic administration of benzo[a]pyrene induces memory impairment and anxiety-like behavior and increases of NR2B DNA methylation. PLoS One, 11(2), e0149574.
  • Zhang, W., Yang, J., Lv, Y., Li, S., & Qiang, M. (2019). Paternal benzo[a]pyrene exposure alters the sperm DNA methylation levels of imprinting genes in F0 generation mice and their unexposed F1-2 male offspring. Chemosphere, 228, 586–594. https://doi.org/https://doi.org/10.1016/j.chemosphere.2019.04.092
  • Zhang, X. H., Geng, G. L., Su, B., Liang, C. P., Wang, F., & Bao, J. C. (2016). MicroRNA-338-3p inhibits glucocorticoid-induced osteoclast formation through RANKL targeting. Genetic Molecular Research, 15, 1–9.
  • Zhang, Y., Wang, X., Fu, Y., Yin, L., Pu, Y., & Liang, G. (2014). Expression profiling and pathway analysis of microRNA expression in the lungs of mice exposed to long-term, low-dose benzo[a]pyrene. Molecular & Cellular Toxicology, 10(1), 67–74.
  • Zhao, Y., Luo, K., Fan, Z., Huang, C., & Hu, J. (2013). Modulation of benzo[a]pyrene-induced toxic effects in Japanese medaka (Oryzias latipes) by 2, 2′, 4, 4′-tetrabromodiphenyl ether. Environmental Science & Technology, 47(22), 13068–13076.
  • Zhou, Y., Jiang, R., An, L., Wang, H., Cheng, S., Qiong, S., & Weng, Y. (2017). Benzo[a]pyrene impedes self-renewal and differentiation of mesenchymal stem cells and influences fracture healing. Science of the Total Environment, 587, 305–315.

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