The role of NF-κB and AhR transcription factors in lead-induced lung toxicity in human lung cancer A549 cells

References

• Abdullah ML, Hafez MM, Al-Hoshani A, Al-Shabanah O. 2018. Anti-metastatic and anti-proliferative activity of eugenol against triple negative and HER2 positive breast cancer cells. BMC Complement Alternat Med. 18(1):321.
   PubMed Web of Science ®Google Scholar
• Abrams TJ, Lee LB, Murray LJ, Pryer NK, Cherrington JM. 2003. SU11248 inhibits KIT and platelet-derived growth factor receptor beta in preclinical models of human small cell lung cancer. Mol Cancer Ther. 2(5):471–478.
   PubMed Web of Science ®Google Scholar
• Agency for Toxic Substances and Disease Registry (ATSDR). 2017. The ATSDR 2017 Substance Priority List. Public Health Service; Available from: https://www.atsdr.cdc.gov/spl/index.html
   Google Scholar
• Al Bakheet SA, Attafi IM, Maayah ZH, Abd-Allah AR, Asiri YA, Korashy HM. 2013. Effect of long-term human exposure to environmental heavy metals on the expression of detoxification and DNA repair genes. Environ Pollut. 181:226–232.
   PubMed Web of Science ®Google Scholar
• Ansari MA, Maayah ZH, Bakheet SA, El-Kadi AO, Korashy HM. 2013. The role of aryl hydrocarbon receptor signaling pathway in cardiotoxicity of acute lead intoxication in vivo and in vitro rat model. Toxicology. 306:40–49.
   PubMed Web of Science ®Google Scholar
• Anttila A, Heikkila P, Pukkala E, Nykyri E, Kauppinen T, Hernberg S, Hemminki K. 1995. Excess lung cancer among workers exposed to lead. Scand J Work Environ Health. 21(6):460–469.
   PubMed Web of Science ®Google Scholar
• Beamer CA, Shepherd DM. 2013. Role of the aryl hydrocarbon receptor (AhR) in lung inflammation. Semin Immunopathol. 35(6):693–704.
   PubMed Web of Science ®Google Scholar
• Brauze D, Fijalkiewicz K, Szaumkessel M, Kiwerska K, Bednarek K, Rydzanicz M, Richter J, Grenman R, Jarmuz-Szymczak M. 2014. Diversified expression of aryl hydrocarbon receptor dependent genes in human laryngeal squamous cell carcinoma cell lines treated with β-naphthoflavone. Toxicol Lett. 231(1):99–107.
   PubMed Web of Science ®Google Scholar
• Chen P, Chang H, Chang J, Lin P. 2012. Aryl hydrocarbon receptor in association with RelA modulates IL-6 expression in non-smoking lung cancer. Oncogene. 31(20):2555.
   PubMed Web of Science ®Google Scholar
• Choi EY, Shin KC, Lee J, Kwon TK, Kim S, Park JW. 2015. Treatment with a small synthetic compound, KMU-193, induces apoptosis in A549 human lung carcinoma cells through p53 up-regulation. Asian Pac J Cancer Prev. 16(14):5883–5887.
   PubMedGoogle Scholar
• Choi Y, Park K, Kim I, Kim SD. 2018. Combined toxic effect of airborne heavy metals on human lung cell line A549. Environ Geochem Health. 40(1):271–282.
   PubMed Web of Science ®Google Scholar
• Csavina J, Field J, Taylor MP, Gao S, Landázuri A, Betterton EA, Sáez AE. 2012. A review on the importance of metals and metalloids in atmospheric dust and aerosol from mining operations. Sci Total Environ. 433:58–73.
   PubMed Web of Science ®Google Scholar
• Döhr O, Sinning R, Vogel C, Münzel P, Abel J. 1997. Effect of transforming growth factor-β1 on expression of aryl hydrocarbon receptor and genes of AhGene battery: clues for independent down-regulation in A549 cells. Mol Pharmacol. 51(5):703–710.
   PubMed Web of Science ®Google Scholar
• Farkhondeh T, Boskabady MH, Jalali S, Bayrami G. 2014. The effect of lead exposure on tracheal responsiveness to methacholine and ovalbumin, total and differential white blood cells count, and serum levels of immunoglobulin E, histamine, and cytokines in guinea pigs. Hum Exp Toxicol. 33:325–333.
   PubMed Web of Science ®Google Scholar
• Ghosh S, May MJ, Kopp EB. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol. 16(1):225–260.
   PubMed Web of Science ®Google Scholar
• Hillyer P, Shepard R, Uehling M, Krenz M, Sheikh F, Thayer KR, Huang L, Yan L, Panda D, Luongo C, et al. 2018. Differential responses by human respiratory epithelial cell lines to respiratory syncytial virus reflect distinct patterns of infection control. J Virol. 92(15):2202.
   Web of Science ®Google Scholar
• Hsu HT, Tseng YT, Wong WJ, Liu CM, Lo YC. 2018. Resveratrol prevents nanoparticles-induced inflammation and oxidative stress via downregulation of PKC-alpha and NADPH oxidase in lung epithelial A549 cells. BMC Complement Alternat Med. 18(1):211.
   PubMed Web of Science ®Google Scholar
• Hukkanen J, Lassila A, Paivarinta K, Valanne S, Sarpo S, Hakkola J, Pelkonen O, Raunio H. 2000. Induction and regulation of xenobiotic-metabolizing cytochrome P450s in the human A549 lung adenocarcinoma cell line. Am J Respir Cell Mol Biol. 22(3):360–366.
   PubMed Web of Science ®Google Scholar
• Jaligama S, Patel VS, Wang P, Sallam A, Harding J, Kelley M, Mancuso SR, Dugas TR, Cormier SA. 2018. Radical containing combustion derived particulate matter enhance pulmonary Th17 inflammation via the aryl hydrocarbon receptor. Part Fibre Toxicol. 15(1):20.
   PubMed Web of Science ®Google Scholar
• Jarup L. 2003. Hazards of heavy metal contamination. Br Med Bull. 68:167–182.
   PubMed Web of Science ®Google Scholar
• Jemal A, Torre LA. 2018. The global burden of cancer. In: The American Cancer Society, editor. The American Cancer Society's principles of oncology: prevention to survivorship. Hoboken, NJ: Wiley:pp. 33–44.
   Google Scholar
• Jung HY, Joo HJ, Park JK, Kim YH. 2012. The blocking of c-met signaling induces apoptosis through the increase of p53 protein in lung cancer. Cancer Res Treat. 44(4):251–261.
   PubMed Web of Science ®Google Scholar
• Kimura A, Naka T, Nakahama T, Chinen I, Masuda K, Nohara K, Fujii-Kuriyama Y, Kishimoto T. 2009. Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. J Exp Med. 206(9):2027–2035.
   PubMed Web of Science ®Google Scholar
• Kobayashi S, Okamoto H, Iwamoto T, Toyama Y, Tomatsu T, Yamanaka H, Momohara S. 2008. A role for the aryl hydrocarbon receptor and the dioxin TCDD in rheumatoid arthritis. Rheumatology. 47(9):1317–1322.
   PubMed Web of Science ®Google Scholar
• Korashy HM, Attafi IM, Ansari MA, Assiri MA, Belali OM, Ahmad SF, Al-Alallah IA, Anazi FE, Alhaider AA. 2016a. Molecular mechanisms of cardiotoxicity of gefitinib in vivo and in vitro rat cardiomyocyte: role of apoptosis and oxidative stress. Toxicol Lett. 252:50–61.
   PubMed Web of Science ®Google Scholar
• Korashy HM, Belali OM, Ansar MA, Alharbi NO. 2016b. FoxO3a is essential for the antiproliferative and apoptogenic effects of sunitinib in MDA-MB231 cell line. Anticancer Res. 36:6097–6108.
   PubMed Web of Science ®Google Scholar
• Korashy HM, El-Kadi AO. 2005. Regulatory mechanisms modulating the expression of cytochrome P450 1A1 gene by heavy metals. Toxicol Sci. 88(1):39–51.
   PubMed Web of Science ®Google Scholar
• Korashy HM, El-Kadi AO. 2008. The role of redox-sensitive transcription factors NF-kappaB and AP-1 in the modulation of the Cyp1a1 gene by mercury, lead, and copper. Free Radic Biol Med. 44(5):795–806.
   PubMed Web of Science ®Google Scholar
• Korashy HM, Maayah ZH, Al Anazi FE, Alsaad AM, Alanazi IO, Belali OM, Al-Atawi FO, Alshamsan A. 2017. Sunitinib inhibits breast cancer cell proliferation by inducing apoptosis, cell-cycle arrest and DNA repair while inhibiting NF-κB signaling pathways. Anticancer Res. 37(9):4899–4909.
   PubMed Web of Science ®Google Scholar
• Kumar S, Singh S, Mehta D, Garg RR, Garg ML, Singh N, Mangal PC, Trehan PN. 1991. Effect of automobile exhaust on the distribution of trace elements and its modulation following Fe, Cu, and Zn supplementation. Biol Trace Elem Res. 31(1):51–62.
   PubMed Web of Science ®Google Scholar
• Li N, Song Y, Zhao W, Han T, Lin S, Ramirez O, Liang L. 2016. Small interfering RNA targeting NF-κB attenuates lipopolysaccharide-induced acute lung injury in rats. BMC Physiol. 16(1):7.
   PubMedGoogle Scholar
• Liu CJ, Zhang XL, Luo DY, Zhu WF, Wan HF, Yang JP, Yang XJ, Wan FS. 2015. Exogenous p53 upregulated modulator of apoptosis (PUMA) decreases growth of lung cancer A549 cells. *Asian Pac J Cancer Prev. 16(2):741–746.
   PubMedGoogle Scholar
• Liu CM, Sun YZ, Sun JM, Ma JQ, Cheng C. 2012. Protective role of quercetin against lead-induced inflammatory response in rat kidney through the ROS-mediated MAPKs and NF-kappaB pathway. Biochim Biophys Acta. 1820(10):1693–1703.
   PubMed Web of Science ®Google Scholar
• Lu CF, Yuan XY, Li LZ, Zhou W, Zhao J, Wang YM, Peng SQ. 2015. Combined exposure to nano-silica and lead induced potentiation of oxidative stress and DNA damage in human lung epithelial cells. Ecotoxicol Environ Saf. 122:537–544.
   PubMed Web of Science ®Google Scholar
• Lundstrom NG, Nordberg G, Englyst V, Gerhardsson L, Hagmar L, Jin T, Rylander L, Wall S. 1997. Cumulative lead exposure in relation to mortality and lung cancer morbidity in a cohort of primary smelter workers. Scand J Work Environ Health. 23:24–30.
   PubMed Web of Science ®Google Scholar
• Mathieu M-C, Lapierre I, Brault K, Raymond M. 2001. Aromatic hydrocarbon receptor (AhR)·AhR nuclear translocator-and p53-mediated induction of the murine multidrug resistance mdr1 gene by 3-methylcholanthrene and benzo (a) pyrene in hepatoma cells. J Biol Chem. 276(7):4819–4827.
   PubMed Web of Science ®Google Scholar
• Mu L, Liu L, Niu R, Zhao B, Shi J, Li Y, Swanson M, Scheider W, Su J, Chang S-C, et al. 2013. Indoor air pollution and risk of lung cancer among Chinese female non-smokers. Cancer Causes Control. 24(3):439–450.
   PubMed Web of Science ®Google Scholar
• Nebert DW, Roe AL, Dieter MZ, Solis WA, Yang Y, Dalton TP. 2000. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem Pharmacol. 59(1):65–85.
   PubMed Web of Science ®Google Scholar
• Rahman I, Adcock I. 2006. Oxidative stress and redox regulation of lung inflammation in COPD. Eur Respir J. 28(1):219–242.
   PubMed Web of Science ®Google Scholar
• Rahman I, Gilmour PS, Jimenez LA, MacNee W. 2002. Oxidative stress and TNF-alpha induce histone acetylation and NF-kappaB/AP-1 activation in alveolar epithelial cells: potential mechanism in gene transcription in lung inflammation. Mol Cell Biochem. 234/235(1):239–248.
   Web of Science ®Google Scholar
• Ren Z, Wang L, Cui J, Huoc Z, Xue J, Cui H, Mao Q, Yang R. 2013. Resveratrol inhibits NF-kB signaling through suppression of p65 and IkappaB kinase activities. Die Pharmazie. 68(8):689–694.
   PubMed Web of Science ®Google Scholar
• Revel A, Raanani H, Younglai E, Xu J, Rogers I, Han R, Savouret JF, Casper RF. 2003. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects lung from DNA damage and apoptosis caused by benzo[a]pyrene. J Appl Toxicol. 23(4):255–261.
   PubMed Web of Science ®Google Scholar
• Rivas-Arancibia S, Zimbron LF, Rodriguez-Martinez E, Maldonado PD, Borgonio Perez G, Sepulveda-Parada M. 2015. Oxidative stress-dependent changes in immune responses and cell death in the substantia nigra after ozone exposure in rat. Front Aging Neurosci. 7:65.
   PubMed Web of Science ®Google Scholar
• Samarghandian S, Borji A, Afshari R, Delkhosh MB, Gholami A. 2013. The effect of lead acetate on oxidative stress and antioxidant status in rat bronchoalveolar lavage fluid and lung tissue. Toxicol Mech Methods. 23(6):432–436.
   PubMed Web of Science ®Google Scholar
• Sanchez-Martin FJ, Fernandez-Salguero PM, Merino JM. 2011. Aryl hydrocarbon receptor-dependent induction of apoptosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin in cerebellar granule cells from mouse. J Neurochem. 118:153–162.
   PubMed Web of Science ®Google Scholar
• Shabani A, Rabbani A. 2000. Lead nitrate induced apoptosis in alveolar macrophages from rat lung. Toxicology. 149(2–3):109–114.
   PubMed Web of Science ®Google Scholar
• Singh J, Pritchard DE, Carlisle DL, McLean JA, Montaser A, Orenstein JM, Patierno SR. 1999. Internalization of carcinogenic lead chromate particles by cultured normal human lung epithelial cells: formation of intracellular lead-inclusion bodies and induction of apoptosis. Toxicol Appl Pharmacol. 161(3):240–248.
   PubMed Web of Science ®Google Scholar
• Sohn SW, Jung JW, Lee SY, Kang HR, Park HW, Min KU, Cho SH. 2013. Expression pattern of GSTP1 and GSTA1 in the pathogenesis of asthma. Exp Lung Res. 39(4–5):173–181.
   PubMed Web of Science ®Google Scholar
• Son YO, Lee JC, Hitron JA, Pan J, Zhang Z, Shi X. 2010. Cadmium induces intracellular Ca2+- and H2O2-dependent apoptosis through JNK- and p53-mediated pathways in skin epidermal cell line. Toxicol Sci. 113(1):127–137.
   PubMed Web of Science ®Google Scholar
• Song JS, Sim SY, Hong DP, Dal Rhee S, Song CW, Han SS, Yang SD. 2001. Lead treatment in vitro at early developmental stage of bone marrow-derived macrophages enhances NO production through IL-1beta and IL-6 but not TNF-alpha. Toxicology. 162(1):61–68.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Yamashita C, Zemans RL, Briones N, Van Linden A, Downey GP. 2009. Leukocyte elastase induces lung epithelial apoptosis via a PAR-1-, NF-kappaB-, and p53-dependent pathway. Am J Respir Cell Mol Biol. 41(6):742–755.
   PubMed Web of Science ®Google Scholar
• Tousson E, Rafat BM, Hessien M, El Barbary AA, Sami A. 2011. P53 and Bcl2 apoptosis proteins in meso-2,3-dimercaptosuccinic acid treated lead-intoxicated rabbits. Toxicol Ind Health. 27(3):271–278.
   PubMed Web of Science ®Google Scholar
• Tsay JJ, Tchou-Wong KM, Greenberg AK, Pass H, Rom WN. 2013. Aryl hydrocarbon receptor and lung cancer. Anticancer Res. 33(4):1247–1256.
   PubMed Web of Science ®Google Scholar
• Van Tiem LA, Di Giulio RT. 2011. AHR2 knockdown prevents PAH-mediated cardiac toxicity and XRE- and ARE-associated gene induction in zebrafish (Danio rerio). Toxicol Appl Pharmacol. 254(3):280–287.
   PubMed Web of Science ®Google Scholar
• Vogel CF, Khan EM, Leung PS, Gershwin ME, Chang WW, Wu D, Haarmann-Stemmann T, Hoffmann A, Denison MS. 2014. Cross-talk between aryl hydrocarbon receptor and the inflammatory response a role for nuclear factor-κB. J Biol Chem. 289(3):1866–1875.
   PubMed Web of Science ®Google Scholar
• Vogel CF, Matsumura F. 2009. A new cross-talk between the aryl hydrocarbon receptor and RelB, a member of the NF-κB family. Biochem Pharmacol. 77(4):734–745.
   PubMed Web of Science ®Google Scholar
• Wang CY, Lin YW, Yang JL. 2008. Activation of protein kinase Calpha signaling prevents cytotoxicity and mutagenicity following lead acetate in CL3 human lung cancer cells. Toxicology. 250(1):55–61.
   PubMed Web of Science ®Google Scholar
• Wang SW, Xu Y, Weng YY, Fan XY, Bai YF, Zheng XY, Lou LJ, Zhang F. 2018. Astilbin ameliorates cisplatin-induced nephrotoxicity through reducing oxidative stress and inflammation. Food Chem Toxicol. 114:227–236.
   PubMed Web of Science ®Google Scholar
• Wang YT, Tzeng DW, Wang CY, Hong JY, Yang JL. 2013. APE1/Ref-1 prevents oxidative inactivation of ERK for G1-to-S progression following lead acetate exposure. Toxicology. 305:120–129.
   PubMed Web of Science ®Google Scholar
• Wohak LE, Krais AM, Kucab JE, Stertmann J, Øvrebø S, Seidel A, Phillips DH, Arlt VM. 2016. Carcinogenic polycyclic aromatic hydrocarbons induce CYP1A1 in human cells via a p53-dependent mechanism. Arch Toxicol. 90(2):291–304.
   PubMed Web of Science ®Google Scholar
• Wong O, Harris F. 2000. Cancer mortality study of employees at lead battery plants and lead smelters, 1947–1995. Am J Ind Med. 38(3):255–270.
   PubMed Web of Science ®Google Scholar
• Xu J, Ji L-D, Xu L-H. 2006. Lead-induced apoptosis in PC 12 cells: involvement of p53, Bcl-2 family and caspase-3. Toxicol Lett. 166(2):160–167.
   PubMed Web of Science ®Google Scholar
• Xu J, Lian L-J, Wu C, Wang X-F, Fu W-Y, Xu L-H. 2008. Lead induces oxidative stress, DNA damage and alteration of p53, Bax and Bcl-2 expressions in mice. Food Chem Toxicol. 46(5):1488–1494.
   PubMed Web of Science ®Google Scholar
• Yoshizawa K, Marsh T, Foley JF, Cai B, Peddada S, Walker NJ, Nyska A. 2005. Mechanisms of exocrine pancreatic toxicity induced by oral treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin in female Harlan Sprague–Dawley rats. Toxicol Sci. 85(1):594–606.
   PubMed Web of Science ®Google Scholar
• Yu X, Pan Y, Ma H, Li W. 2013. Simvastatin inhibits proliferation and induces apoptosis in human lung cancer cells. Oncol Res. 20(8):351–357.
   PubMed Web of Science ®Google Scholar
• Zeng X, Xu X, Boezen HM, Vonk JM, Wu W, Huo X. 2017. Decreased lung function with mediation of blood parameters linked to e-waste lead and cadmium exposure in preschool children. Environ Pollut. 230:838–848.
   PubMed Web of Science ®Google Scholar
• Zhang D, Ma D, Yao Z, Fu C, Shi Y, Wang Q, Tang Q. 2016. ERK1/2/p53 and NF-κB dependent-PUMA activation involves in doxorubicin-induced cardiomyocyte apoptosis. Eur Rev Med Pharmacol Sci. 20(11):2435–2442.
   PubMed Web of Science ®Google Scholar
• Zhang S, Patel A, Chu C, Jiang W, Wang L, Welty SE, Moorthy B, Shivanna B. 2015. Aryl hydrocarbon receptor is necessary to protect fetal human pulmonary microvascular endothelial cells against hyperoxic injury: mechanistic roles of antioxidant enzymes and RelB. Toxicol Appl Pharmacol. 286(2):92–101.
   PubMed Web of Science ®Google Scholar
• Zhao H, Barger MW, Ma JK, Castranova V, Ma JY. 2006. Cooperation of the inducible nitric oxide synthase and cytochrome P450 1A1 in mediating lung inflammation and mutagenicity induced by diesel exhaust particles. Environ Health Perspect. 114(8):1253–1258.
   PubMed Web of Science ®Google Scholar
• Zhao H, Wang Y, Shao Y, Liu J, Wang S, Xing M. 2018. Oxidative stress-induced skeletal muscle injury involves in NF-kappaB/p53-activated immunosuppression and apoptosis response in copper (II) or/and arsenite-exposed chicken. Chemosphere. 210:76–84.
   PubMed Web of Science ®Google Scholar