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Ameliorative effect of boric acid against nicotine-induced cytotoxicity on cultured human primary alveolar epithelial cells

Year 2016, Volume: 1 Issue: 2, 104 - 109, 09.09.2016

Abstract

Nearly six million people die from smoking due to addiction to nicotine. Because of high toxicity by nicotine, main alkaloid in tobacco, the action modes of nicotine have been analyzed comprehensively by scientists in different organisms and cell cultures. One of the main cytotoxicity mechanisms of nicotine is that activating lipid peroxidation by inducing production of reactive oxygen species (ROS). Recent investigations support that boric acid exhibits cyto-protective properties on different cell types via its antioxidant nature. Thus, in this study BA was assessed as a potential cyto-protective agent against nicotine-induced cytotoxicity. Therefore, toxic concentrations of nicotine were evaluated on human primary alveolar epithelial cells (HPAEpiC) and BA was applied against toxic dose of nicotine to analyze whether cytotoxicity could be attenuated or not. Wide spectrum nicotine hydrogen tartrate concentrations (0.312 mM to 20 mM) were used to investigate the cytotoxicity. 3-(4,5-dimethyl-thiazol-2-yl) 2,5-diphenyltetrazolium bromide (MTT) and lactate dehydrogenase (LDH) release assays were used to analyze cytotoxicity after exposure to nicotine and boric acid, and thier combinations. In addition, Hoechst 33258 (bis-Benzimide) dye was used to analyze genome integrity under fluorescent microscope.  According to the results of MTT cell viability assay, IC50 concentration of nicotine was determined as 1.71 mM. Different concentration of BA (0.625 µg/ml to 20 µg/ml) were applied into cultured HPAEpiC cells with nicotine to prevent cellular damages by nicotine. MTT and LDH assays clearly showed that 5 µg/ml of BA supplementation increased cell viability against nicotine exposure. Again, Hoechst 33258 test revealed that chromosome structure was preserved significantly after BA exposure.  As a conclusion, our results revealed for the first time that BA could be used as a protective agent against nicotine-induced toxicity on human lung alveolar cells.

References

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  • Turkez, H. Effects of boric acid and borax on titanium dioxide genotoxicity. J. Appl. Toxicol. 28, 658–664, 2008.
  • Rao, P., Ande, A., Sinha, N., Kumar, A. & Kumar, S. Effects of Cigarette Smoke Condensate on Oxidative Stress, Apoptotic Cell Death, and HIV Replication in Human Monocytic Cells. PLoS One 11, e0155791, 2016.
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  • Tanni, S. E. et al. Increased production of hydrogen peroxide by peripheral blood monocytes associated with smoking exposure intensity in smokers. J. Inflamm. (Lond). 9, 45, 2012.
  • Facchinetti, F. et al. Alpha,beta-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am. J. Respir. Cell Mol. Biol. 37, 617–23, 2007.
  • Newman, M. B. et al. Nicotine’s oxidative and antioxidant properties in CNS. Life Sci. 71, 2807–2820, 2002.
  • Tepedelen, B. E., Soya, E. & Korkmaz, M. Boric Acid Reduces the Formation of DNA Double Strand Breaks and Accelerates Wound Healing Process. Biol. Trace Elem. Res.. doi:10.1007/s12011-016-0729-9, 2016.
  • Zhao, Z. & Reece, E. A. Nicotine-induced embryonic malformations mediated by apoptosis from increasing intracellular calcium and oxidative stress. Birth Defects Res. Part B - Dev. Reprod. Toxicol. 74, 383–391, 2005.
  • Jang, M.-H. et al. Alcohol and nicotine reduce cell proliferation and enhance apoptosis in dentate gyrus. Neuroreport 13, 1509–13, 2002.
  • Crowley-Weber, C. L. et al. Nicotine increases oxidative stress, activates NF-κB and GRP78, induces apoptosis and sensitizes cells to genotoxic/xenobiotic stresses by a multiple stress inducer, deoxycholate: relevance to colon carcinogenesis. Chem. Biol. Interact. 145, 53–66, 2003.
  • Sudheer, A. R., Muthukumaran, S., Devipriya, N., Devaraj, H. & Menon, V. P. Influence of ferulic acid on nicotine-induced lipid peroxidation, DNA damage and inflammation in experimental rats as compared to N-acetylcysteine. Toxicology 243, 317–29, 2008.
  • Ustündağ, A., Behm, C., Föllmann, W., Duydu, Y. & Degen, G. H. Protective effect of boric acid on lead- and cadmium-induced genotoxicity in V79 cells. Arch. Toxicol. 88, 1281–9, 2014.
  • Ince, S., Kucukkurt, I., Cigerci, I. H., Fatih Fidan, A. & Eryavuz, A. The effects of dietary boric acid and borax supplementation on lipid peroxidation, antioxidant activity, and DNA damage in rats. J. Trace Elem. Med. Biol. 24, 161–164, 2010.
Year 2016, Volume: 1 Issue: 2, 104 - 109, 09.09.2016

Abstract

References

  • Zinck, S. E., Leung, A. N., Frost, M., Berry, G. J. & Müller, N. L. Pulmonary cryptococcosis: CT and pathologic findings. J. Comput. Assist. Tomogr. 26, 330–4, 2002.
  • Matalon, S., Holm, B. A., Baker, R. R., Whitfield, M. K. & Freeman, B. A. Characterization of antioxidant activities of pulmonary surfactant mixtures. Biochim. Biophys. Acta - Gen. Subj. 1035, 121–127, 1990.
  • Holden, W. E., Maier, J. M. & Malinow, M. R. Cigarette smoke extract increases albumin flux across pulmonary endothelium in vitro. J. Appl. Physiol. 66, 443–9, 1989.
  • Simon, R. H., Scott, M. J., Reza, M. M. & Killen, P. D. Type IV collagen production by rat pulmonary alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 8, 640–6, 1993.
  • Hoshino, Y. et al. Cytotoxic effects of cigarette smoke extract on an alveolar type II cell-derived cell line. Am. J. Physiol. Lung Cell. Mol. Physiol. 281, L509–16, 2001.
  • Leanderson, P. & Tagesson, C. Cigarette smoke-induced DNA damage in cultured human lung cells: Role of hydroxyl radicals and endonuclease activation. Chem. Biol. Interact. 81, 197–208, 1992.
  • Lannan, S., Donaldson, K., Brown, D. & MacNee, W. Effect of cigarette smoke and its condensates on alveolar epithelial cell injury in vitro. Am. J. Physiol. 266, L92–L100, 1994.
  • Hoffmann, D. & Adams, J. D. Carcinogenic tobacco-specific N-nitrosamines in Snuff and in the saliva of snuff dippers. Cancer Res. 41, 4305–4308, 1981.
  • Cuff, M. J., McQuade, M. J., Scheidt, M. J., Sutherland, D. E. & Van Dyke, T. E. The presence of nicotine on root surfaces of periodontally diseased teeth in smokers. J. Periodontol. 60, 564–9, 1989.
  • Hanes, P. J., Schuster, G. S. & Lubas, S. Binding, uptake, and release of nicotine by human gingival fibroblasts. J Periodontol 62, 147–152, 1991.
  • Chang, Y. C., Lii, C. K., Tai, K. W. & Chou, M. Y. Adverse effects of arecoline and nicotine on human periodontal ligament fibroblasts in vitro. J. Clin. Periodontol. 28, 277–82, 2001.
  • Chang, Y.-C., Huang, F.-M., Tai, K.-W., Yang, L.-C. & Chou, M.-Y. Mechanisms of cytotoxicity of nicotine in human periodontal ligament fibroblast cultures in vitro. J. Periodontal Res. 37, 279–285, 2002.
  • Avino-Martinez, J. A., Espana-Gregori, E., Peris-Martinez, C. P. & Blanes, M. Successful boric acid treatment of Aspergillus niger infection in an exenterated orbit. Ophthal. Plast. Reconstr. Surg. 24, 79–81, 2008.
  • Devirian, T. A. & Volpe, S. L. The physiological effects of dietary boron. Crit. Rev. Food Sci. Nutr. 43, 219–231, 2003.
  • Yılmaz, B. & Evis, Z. Boron-Substituted Bioceramics: A Review. J. Boron 1, 6–14, 2016.
  • Turkez, H., Tatar, A., Hacimuftuoglu, A. & Ozdemir, E. Boric acid as a protector against paclitaxel genotoxicity. Acta Biochim. Pol. 57, 95–97, 2010.
  • Turkez, H. Effects of boric acid and borax on titanium dioxide genotoxicity. J. Appl. Toxicol. 28, 658–664, 2008.
  • Rao, P., Ande, A., Sinha, N., Kumar, A. & Kumar, S. Effects of Cigarette Smoke Condensate on Oxidative Stress, Apoptotic Cell Death, and HIV Replication in Human Monocytic Cells. PLoS One 11, e0155791, 2016.
  • Lerner, L., Weiner, D., Katz, R., Reznick, A. Z. & Pollack, S. Increased pro-inflammatory activity and impairment of human monocyte differentiation induced by in vitro exposure to cigarette smoke. J. Physiol. Pharmacol. 60 Suppl 5, 81–86, 2009.
  • Suzuki, M. et al. Down-regulated NF-E2-related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 39, 673–682, 2008.
  • Tanni, S. E. et al. Increased production of hydrogen peroxide by peripheral blood monocytes associated with smoking exposure intensity in smokers. J. Inflamm. (Lond). 9, 45, 2012.
  • Facchinetti, F. et al. Alpha,beta-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am. J. Respir. Cell Mol. Biol. 37, 617–23, 2007.
  • Newman, M. B. et al. Nicotine’s oxidative and antioxidant properties in CNS. Life Sci. 71, 2807–2820, 2002.
  • Tepedelen, B. E., Soya, E. & Korkmaz, M. Boric Acid Reduces the Formation of DNA Double Strand Breaks and Accelerates Wound Healing Process. Biol. Trace Elem. Res.. doi:10.1007/s12011-016-0729-9, 2016.
  • Zhao, Z. & Reece, E. A. Nicotine-induced embryonic malformations mediated by apoptosis from increasing intracellular calcium and oxidative stress. Birth Defects Res. Part B - Dev. Reprod. Toxicol. 74, 383–391, 2005.
  • Jang, M.-H. et al. Alcohol and nicotine reduce cell proliferation and enhance apoptosis in dentate gyrus. Neuroreport 13, 1509–13, 2002.
  • Crowley-Weber, C. L. et al. Nicotine increases oxidative stress, activates NF-κB and GRP78, induces apoptosis and sensitizes cells to genotoxic/xenobiotic stresses by a multiple stress inducer, deoxycholate: relevance to colon carcinogenesis. Chem. Biol. Interact. 145, 53–66, 2003.
  • Sudheer, A. R., Muthukumaran, S., Devipriya, N., Devaraj, H. & Menon, V. P. Influence of ferulic acid on nicotine-induced lipid peroxidation, DNA damage and inflammation in experimental rats as compared to N-acetylcysteine. Toxicology 243, 317–29, 2008.
  • Ustündağ, A., Behm, C., Föllmann, W., Duydu, Y. & Degen, G. H. Protective effect of boric acid on lead- and cadmium-induced genotoxicity in V79 cells. Arch. Toxicol. 88, 1281–9, 2014.
  • Ince, S., Kucukkurt, I., Cigerci, I. H., Fatih Fidan, A. & Eryavuz, A. The effects of dietary boric acid and borax supplementation on lipid peroxidation, antioxidant activity, and DNA damage in rats. J. Trace Elem. Med. Biol. 24, 161–164, 2010.
There are 30 citations in total.

Details

Journal Section Research Article
Authors

Mehmet Enes Arslan

Hasan Türkez This is me

Özlem Özdemir This is me

Olfa Chikha This is me

Publication Date September 9, 2016
Published in Issue Year 2016 Volume: 1 Issue: 2

Cite

APA Arslan, M. E., Türkez, H., Özdemir, Ö., Chikha, O. (2016). Ameliorative effect of boric acid against nicotine-induced cytotoxicity on cultured human primary alveolar epithelial cells. Journal of Boron, 1(2), 104-109.

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TENMAK Boron Research Institute