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Review

Toxic and carcinogenic effects of hexavalent chromium in mammalian cells in vivo and in vitro: a recent update

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References

  • Avudainayagam S, Megharaj M, Owens G, et al. Chemistry of chromium in soils with emphasis on tannery waste sites. In Ware GW, ed. Reviews of Environmental Contamination and Toxicology. Vol. 178. New York: Springer; 2003. p. 53–91. doi:10.1007/0-387-21728-2_3.
  • Babula P, Adam V, Opatrilova R, et al. Uncommon heavy metals, metalloids and their plant toxicity: a review. In: Lichtfouse E, ed. Organic Farming, Pest Control and Remediation of Soil Pollutants. Vol. 1. Dordrecht: Springer; 2009. p. 275–317. doi:10.1007/978-1-4020-9654-9_14.
  • Zhitkovich A. Chromium in drinking water: sources, metabolism, and cancer risks. Chem Res Toxicol. 2011;24(10):1617–1629. doi:10.1021/tx200251t.
  • DesMarais TL, Costa M. Mechanisms of chromium-induced toxicity. Curr Opin Toxicol. 2019;14:1–7. doi:10.1016/j.cotox.2019.05.003.
  • Cheng Y, Holman HY, Lin Z. Remediation of chromium and uranium contamination by microbial activity. Elements. 2012;8(2):107–112. doi:10.2113/gselements.8.2.107.
  • Das AP, Singh S. Occupational health assessment of chromite toxicity among Indian miners. Indian J Occup Environ Med. 2011;15(1):6–13. doi:10.4103/0019-5278.82998.
  • Zayed AM, Terry N. Chromium in the environment: factors affecting biological remediation. Plant Soil. 2003;249(1):139–156. doi:10.1023/A:1022504826342..
  • WHO. Guidelines for drinking-water quality. 2003. 2.
  • Rieuwerts J. Chromium. In: The Elements of Environmental Pollution. Vol 3. London: Routledge; 2017. p. 198–205. doi:10.4324/9780203798690-10.
  • Aldmour ST, Burke IT, Bray AW, et al. Abiotic reduction of Cr(VI) by humic acids derived from peat and lignite: kinetics and removal mechanism. Environ Sci Pollut Res Int. 2019;26(5):4717–4729. doi:10.1007/s11356-018-3902-1.
  • Powell RM, Puls RW, Hightower SK, Sabatini DA. Coupled iron corrosion and chromate reduction: mechanisms for subsurface remediation. Environ Sci Technol. 1995;29(8):1913–1922. doi:10.1021/es00008a008.
  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy metal toxicity and the environment. In: Luch A, edMolecular, Clinical and Environmental Toxicology. Experientia Supplementum. Vol101. Basel: Springer; 2012. p. 133–164. doi:10.1007/978-3-7643-8340-4_6.
  • Vincent JB. The potential value and toxicity of chromium picolinate as a nutritional supplement, weight loss agent and muscle development agent. Sports Med. 2003;33(3):213–230. doi:10.2165/00007256-200333030-00004.
  • Bell SJ, Goodrick GK. A functional food product for the management of weight. Crit Rev Food Sci Nutr. 2002;42(2):163–178. doi:10.1080/10408690290825501.
  • Dhatrak SV, Nandi SS. Risk assessment of chronic poisoning among Indian metallic miners. Indian J Occup Environ Med. 2009;13(2):60–64. doi:10.4103/0019-5278.55121.
  • Deepali KKG. Metals concentration in textile and tannery effluents, associated soils and ground water. New York Sci J. 2010;3(4):82–89.
  • Gopalakrishnan K, Jeyadoss T. Comparative study on biosorption of Zn(II), Cu(II) and Cr(VI) from textile dye effluent using activated rice husk and activated coconut fibre. Indian J Chem Technol. 2011;18(1):61–66.
  • Chandra R, Pandey PK, Srivastava A. Comparative toxicological evaluation of untreated and treated tannery effluent with Nostoc muscorum L. (algal assay) and microtox bioassay. Environ Monit Assess. 2004;95(1-3):287–294. doi:10.1023/B:EMAS.0000029909.87977.a5.
  • Sinha S, Gupta AK, Bhatt K, et al. Distribution of metals in the edible plants grown at Jajmau, Kanpur (India) receiving treated tannery wastewater: relation with physico-chemical properties of the soil. Environ Monit Assess. 2006;115(1-3):1–22. doi:10.1007/s10661-006-5036-z.
  • Dhungana TP, Yadav PN. Determination of chromium in tannery effluent and study of adsorption of Cr (VI) on saw dust and charcoal from sugarcane bagasses. J. Nepal Chem. Soc. 1970;23:93–101. doi:10.3126/jncs.v23i0.2102.
  • Appiah-Brempong M, Essandoh HMK, Asiedu NY, et al. Artisanal tannery wastewater: quantity and characteristics. Heliyon. 2022;8(1):e08680. doi:10.1016/j.heliyon.2021.e08680.
  • Ganesh R, Ramanujam RA. Biological waste management of leather tannery effluents in India: current options and future research needs. IJEE. 2009;1(2):165. doi:10.1504/IJEE.2009.027313.
  • Singh RK, Sengupta B, Bali R, et al. Identification and mapping of chromium (VI) plume in groundwater for remediation: a case study at Kanpur, Uttar Pradesh. J Geol Soc India. 2009;74(1):49–57. doi:10.1007/s12594-009-0103-z.
  • Dotaniya ML, Meena VD, Rajendiran S, et al. Geo-accumulation indices of heavy metals in soil and groundwater of Kanpur, India under long term irrigation of tannery effluent. Bull Environ Contam Toxicol. 2017;98(5):706–711. doi:10.1007/s00128-016-1983-4.
  • Mondal NC, Singh VP. Hydrochemical analysis of salinization for a tannery belt in southern India. J Hydrol. 2011;405(3-4):235–247. doi:10.1016/j.jhydrol.2011.05.058.
  • Sanyal T, Kaviraj A, Saha S. Deposition of chromium in aquatic ecosystem from effluents of handloom textile industries in Ranaghat-Fulia region of West Bengal, India. J Adv Res. 2015;6(6):995–1002. doi:10.1016/j.jare.2014.12.002.
  • Pal S, Chakraborty S, Chattopadhay B, et al. Leather industries of kolkata vis-à-vis present status of Cr 3+ and Cr 6+ contents in physical environment of east Kolkata wetlands. J Indian Leather Technol Assoc. 2018;(October):17–23.
  • Kanagaraj G, Elango L. Chromium and fluoride contamination in groundwater around leather tanning industries in southern India: Implications from stable isotopic ratio δ53Cr/δ 52Cr, Geochemical and Geostatistical Modelling. Chemosphere. 2019;220:943–953. doi:10.1016/j.chemosphere.2018.12.105.
  • Princy S, Sathish SS, Cibichakravarthy B, Prabagaran SR. Hexavalent chromium reduction by Morganella morganii (1AB1) isolated from tannery effluent contaminated sites of Tamil Nadu, India. Biocatal Agric Biotechnol. 2020;23:101469. doi:10.1016/j.bcab.2019.101469.
  • Karunanidhi D, Aravinthasamy P, Subramani T, et al. Chromium contamination in groundwater and sobol sensitivity model based human health risk evaluation from leather tanning industrial region of south India. Environ Res. 2021;199(January):111238. doi:10.1016/j.envres.2021.111238.
  • Mishra S, Das AP, Seragadam P. Microbial remediation of hexavalent chromium from chromite contaminated mines of Sukinda valley, Orissa (India). J Env Res Dev. 2009;3:1122–1127.
  • Nayak S, S R, P B, Kale P. A review of chromite mining in Sukinda valley of India: impact and potential remediation measures. Int J Phytoremediation. 2020;22(8):804–818. doi:10.1080/15226514.2020.1717432.
  • Shanker AK, Venkateswarlu B. Chromium: environmental pollution, health effects and mode of action. In Nriagu JO, ed. Encyclopedia of Environmental Health. Burlington. Elsevier; 2011. p. 650–659. doi:10.1016/B978-0-444-52272-6.00390-1.
  • Stankovic S, Kalaba P, Stankovic AR. Biota as toxic metal indicators. Environ Chem Lett. 2014;12(1):63–84. doi:10.1007/s10311-013-0430-6.
  • U.S Environmental Protection Agenc. Data summary of the third unregulated contaminant monitoring rule. https://www.epa.gov/sites/production/files/2017-02/documents/ucmr3-data-summary-january-2017.pdf. 2017. 12.
  • McNeill LS, McLean JE, Parks JL, Edwards MA. Hexavalent chromium review, part 2: chemistry, occurrence, and treatment. J Am Water Works Assoc. 2012;104(7):E395–E405. doi:10.5942/jawwa.2012.104.0092.
  • Schaffner IR, Singh RK, Lamb SR, Kirkland DN. Enhanced bioremediation pilot study of a Cr(VI)-impacted overburden groundwater system in Kanpur, Uttar Pradesh, India. Assoc Environ Heal Sci - 23rd Annu Int Conf Soils, Sediments Water 2007. 2007;13(January):59–70.
  • Izbicki JA, Wright MT, Seymour WA, et al. Cr(VI) occurrence and geochemistry in water from public-supply wells in california. Appl Geochemistry. 2015;63:203–217. doi:10.1016/j.apgeochem.2015.08.007.
  • Linos A, Petralias A, Christophi CA, et al. Oral ingestion of hexavalent chromium through drinking water and cancer mortality in an industrial area of Greece-an ecological study. Environ Health. 2011;10:50. doi:10.1186/1476-069X-10-50.
  • Salnikow K, Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic, and chromium. Chem Res Toxicol. 2008;21(1):28–44. doi:10.1021/tx700198a.
  • Proctor DM, Otani JM, Finley BL, et al. Is hexavalent chromium carcinogenic via ingestion? a weight-of-evidence review. J Toxicol Environ Health A. 2002;65(10):701–746. doi:10.1080/00984100290071018.
  • O'Brien TJ, Ceryak S, Patierno SR. Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat Res. 2003;533(1-2):3–36. doi:10.1016/j.mrfmmm.2003.09.006.
  • Yao H, Guo L, Jiang B-H, Luo J, Shi X. Oxidative stress and chromium(VI) carcinogenesis. J Environ Pathol Toxicol Oncol. 2008;27(2):77–88. doi:10.1615/jenvironpatholtoxicoloncol.v27.i2.10.
  • Stearns DM, Kennedy LJ, Courtney KD, Giangrande PH, Phieffer LS, Wetterhahn KE. Reduction of chromium(VI) by ascorbate leads to chromium-DNA binding and DNA strand breaks in vitro. Biochemistry. 1995;34(3):910–919. doi:10.1021/bi00003a025.
  • Nickens KP, Patierno SR, Ceryak S. Chromium genotoxicity: a double-edged sword. Chem Biol Interact. 2010;188(2):276–288. doi:10.1016/j.cbi.2010.04.018.
  • Sun H, Brocato J, Costa M. Oral chromium exposure and toxicity. Curr Environ Health Rep. 2015;2(3):295–303. doi:10.1007/s40572-015-0054-z.
  • Chiu A, Shi XL, Lee WKP, et al. Review of chromium (VI) apoptosis, cell-cycle-arrest, and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2010;28(3):188–230. doi:10.1080/10590501.2010.504980.
  • De Flora S, Bagnasco M, Serra D, Zanacchi P. Genotoxicity of chromium compounds. a review. Mutat Res Genet Toxicol. 1990;238(2):99–172. doi:10.1016/0165-1110(90)90007-X.
  • Xie Y, Holmgren S, Andrews DMK, Wolfe MS. Evaluating the impact of the U.S. national toxicology program: a case study on hexavalent chromium. Environ Health Perspect. 2017;125(2):181–188. doi:10.1289/EHP21.
  • Costa M. Toxicity and carcinogenicity of Cr(VI) in animal models and humans. Crit Rev Toxicol. 1997;27(5):431–442. doi:10.3109/10408449709078442.
  • Belyaeva EA, Dymkowska D, Wieckowski MR, Wojtczak L. Mitochondria as an important target in heavy metal toxicity in rat hepatoma AS-30D cells. Toxicol Appl Pharmacol. 2008;231(1):34–42. doi:10.1016/j.taap.2008.03.017.
  • Wang C, Youle RJ. The role of mitochondria in apoptosis. Annu Rev Genet. 2009;43:95–118. doi:10.1146/annurev-genet-102108-134850.
  • Tait SWG, Green DR. Mitochondria and cell signalling. J Cell Sci. 2012;125(Pt 4):807–815. doi:10.1242/jcs.099234.
  • Valko M, Morris H, Cronin MTD. Metals, toxicity and oxidative stress. Curr Med Chem. 2005;12(10):1161–1208. doi:10.2174/0929867053764635.
  • Valko M, Rhodes CJ, Moncol J, et al. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160(1):1–40. doi:10.1016/j.cbi.2005.12.009.
  • Xiao F, Li Y, Luo L, et al. Role of mitochondrial electron transport chain dysfunction in Cr(VI)-induced cytotoxicity in L-02 hepatocytes. Cell Physiol Biochem. 2014;33(4):1013–1025. doi:10.1159/000358672.
  • Ge H, Li Z, Jiang L, et al. Cr (VI) induces crosstalk between apoptosis and autophagy through endoplasmic reticulum stress in A549 cells. Chem Biol Interact. 2019;298:35–42. doi:10.1016/j.cbi.2018.10.024.
  • Soares ME, Vieira E, Bastos M de L. Chromium speciation analysis in bread samples. J Agric Food Chem. 2010;58(2):1366–1370. doi:10.1021/jf903118v.
  • DeLoughery Z, Luczak MW, Zhitkovich A. Monitoring Cr intermediates and reactive oxygen species with fluorescent probes during chromate reduction. Chem Res Toxicol. 2014;27(5):843–851. doi:10.1021/tx500028x.
  • Quievryn G, Goulart M, Messer J, Zhitkovich A. Reduction of Cr (VI) by cysteine: significance in human lymphocytes and formation of DNA damage in reactions with variable reduction rates. Mol Cell Biochem. 2001;222(1-2):107–118.
  • Sugden KD, Stearns DM. The role of chromium(V) in the mechanism of chromate-induced oxidative DNA damage and cancer. J Environ Pathol Toxicol Oncol. 2000;19(3):215–230.
  • Travacio M, Marı́a Polo J, Llesuy S. Erratum to “chromium (VI) induces oxidative stress in the mouse brain. Toxicology. 2001;162(2):139–148. doi:10.1016/S0300-483X(00)00423-6.
  • Li X, He S, Zhou J, et al. Cr (VI) induces abnormalities in glucose and lipid metabolism through ROS/Nrf2 signaling. Ecotoxicol Environ Saf. 2021;219:112320. doi:10.1016/j.ecoenv.2021.112320.
  • Jin Y, Zhang S, Tao R, et al. Oral exposure of mice to cadmium (II), chromium (VI) and their mixture induce oxidative- and endoplasmic reticulum-stress mediated apoptosis in the livers. Environ Toxicol. 2016;31(6):693–705. doi:10.1002/tox.22082.
  • Kalayarasan S, Sriram N, Sureshkumar A, Sudhandiran G. Chromium (VI)-induced oxidative stress and apoptosis is reduced by garlic and its derivative s-allylcysteine through the activation of Nrf2 in the hepatocytes of Wistar rats. J Appl Toxicol. 2008;28(7):908–919. doi:10.1002/jat.1355.
  • Molina-Jijón E, Tapia E, Zazueta C, et al. Curcumin prevents Cr(VI)-induced renal oxidant damage by a mitochondrial pathway. Free Radic Biol Med. 2011;51(8):1543–1557. doi:10.1016/j.freeradbiomed.2011.07.018.
  • Luczak MW, Green SE, Zhitkovich A. Different ATM signaling in response to chromium(VI) metabolism via ascorbate and nonascorbate reduction: implications for in vitro models and toxicogenomics. Environ Health Perspect. 2016;124(1):61–66. doi:10.1289/ehp.1409434.
  • Acharya UR, Mishra M, Tripathy RR, Mishra I. Testicular dysfunction and antioxidative defense system of Swiss mice after chromic acid exposure. Reprod Toxicol. 2006;22(1):87–91. doi:10.1016/j.reprotox.2005.11.004.
  • Anand SS. Protective effect of vitamin B6 in chromium-induced oxidative stress in liver. J Appl Toxicol. 2005;25(5):440–443. doi:10.1002/jat.1077.
  • Chandra AK, Chatterjee A, Ghosh R, Sarkar M. Effect of curcumin on chromium-induced oxidative damage in male reproductive system. Environ Toxicol Pharmacol. 2007;24(2):160–166. doi:10.1016/j.etap.2007.04.009.
  • Hu G, Li P, Cui X, et al. Cr(VI)-induced methylation and down-regulation of DNA repair genes and its association with markers of genetic damage in workers and 16HBE cells. Environ Pollut. 2018;238:833–843. doi:10.1016/j.envpol.2018.03.046.
  • Hu G, Li P, Li Y, et al. Methylation levels of p16 and tp53 that are involved in DNA strand breakage of 16HBE cells treated by hexavalent chromium. Toxicol Lett. 2016;249:15–21. doi:10.1016/j.toxlet.2016.03.003.
  • Ali AHK, Kondo K, Namura T, et al. Aberrant DNA methylation of some tumor suppressor genes in lung cancers from workers with chromate exposure. Mol Carcinog. 2011;50(2):89–99. doi:10.1002/mc.20697.
  • Chen QY, Murphy A, Sun H, Costa M. Molecular and epigenetic mechanisms of Cr(VI)-induced carcinogenesis. Toxicol Appl Pharmacol. 2019;377:114636. doi:10.1016/j.taap.2019.114636.
  • Quievryn G, Peterson E, Messer J, Zhitkovich A. Genotoxicity and mutagenicity of chromium(VI)/ascorbate-generated DNA adducts in human and bacterial cells. Biochemistry. 2003;42(4):1062–1070. doi:10.1021/bi0271547.
  • Arakawa H, Weng MW, Chen WC, Tang M. Chromium (VI) induces both bulky DNA adducts and oxidative DNA damage at adenines and guanines in the p53 gene of human lung cells. Carcinogenesis. 2012;33(10):1993–2000. doi:10.1093/carcin/bgs237.
  • Lakin ND, Jackson SP. Regulation of p53 in response to DNA damage. Oncogene. 1999;18(53):7644–7655. doi:10.1038/sj.onc.1203015.
  • Luczak MW, Krawic C, Zhitkovich A. p53 activation by Cr(VI): a transcriptionally limited response induced by ATR kinase in s-phase. Toxicol Sci. 2019;172(1):11–22. doi:10.1093/toxsci/kfz178.
  • Thompson CM, Seiter J, Chappell MA, et al. Synchrotron-based imaging of chromium and γ-H2AX immunostaining in the duodenum following repeated exposure to Cr(VI) in drinking water. Toxicol Sci. 2015;143(1):16–25. doi:10.1093/toxsci/kfu206.
  • Patiemo SR, Banh D, Landolph JR. Transformation of C3H/10T1/2 mouse embryo cells to focus formation and anchorage independence by insoluble lead chromate but not soluble calcium chromate: relationship to mutagenesis and internalization of lead chromate particles. Cancer Res. 1988;48(18):5280–5288.
  • Holmes AL, Wise SS, Wise JPS. Carcinogenicity of hexavalent chromium. Indian J Med Res. 2008;128(4):353–372.
  • O'Brien TJ, Ding H, Suh M, et al. Assessment of K-Ras mutant frequency and micronucleus incidence in the mouse duodenum following 90-days of exposure to Cr(VI) in drinking water. Mutat Res. 2013;754(1-2):15–21. doi:10.1016/j.mrgentox.2013.03.008.
  • Zeidler-Erdely PC, Falcone LM, Antonini JM, et al. Tumorigenic response in lung tumor susceptible A/J mice after sub-chronic exposure to calcium chromate or iron (III) oxide. Toxicol Lett. 2020;334:60–65. doi:10.1016/j.toxlet.2020.09.012.
  • Zhang Z, Cao H, Song N, et al. Long-term hexavalent chromium exposure facilitates colorectal cancer in mice associated with changes in gut microbiota composition. Food Chem Toxicol. 2020;138(February):111237. doi:10.1016/j.fct.2020.111237.
  • Mezencev R, Auerbach SS. Inferred inactivation of the Cftr gene in the duodena of mice exposed to hexavalent chromium (Cr(VI)) in drinking water supports its tumor-suppressor status and implies its potential role in Cr(VI)-induced carcinogenesis of the small intestines. Toxicol Appl Pharmacol. 2021;433(June):115773. doi:10.1016/j.taap.2021.115773.
  • Xia B, Yang L, Huang H, et al. Chromium(VI) causes down regulation of biotinidase in human bronchial epithelial cells by modifications of histone acetylation. Toxicol Lett. 2011;205(2):140–145. doi:10.1016/j.toxlet.2011.05.1032.
  • Lee YH, Su SB, Huang CC, et al. N-acetylcysteine attenuates hexavalent chromium-induced hypersensitivity through inhibition of cell death, ROS-related signaling and cytokine expression. PLoS One. 2014;9(9):e108317. doi:10.1371/journal.pone.0108317.
  • Klein CB, Su L, Bowser D, Leszczynska J. Chromate-induced epimutations in mammalian cells. Environ Health Perspect. 2002;110(Suppl 5):739–743. doi:10.1289/ehp.02110s5739.
  • Zhang R, Xiang Y, Ran Q, et al. Involvement of calcium, reactive oxygen species, and ATP in hexavalent chromium-induced damage in red blood cells. Cell Physiol Biochem. 2014;34(5):1780–1791. doi:10.1159/000366378.
  • Xia H, Ying S, Feng L, et al. Decreased 8-oxoguanine DNA glycosylase 1 (hogg1) expression and DNA oxidation damage induced by Cr (VI). Chem Biol Interact. 2019;299:44–51. doi:10.1016/j.cbi.2018.11.019.
  • Liang Q, Xiao Y, Liu K, et al. Cr(VI)-induced autophagy protects L-02 hepatocytes from apoptosis through the ROS-Akt-mTOR pathway. Cell Physiol Biochem. 2018;51(4):1863–1878. doi:10.1159/000495713.
  • Liu K, Chen P, Lu J, et al. Protective effect of purple tomato anthocyanidin on chromium(VI)-induced autophagy in LMH cells by inhibiting endoplasmic reticulum stress. Biol Trace Elem Res. 2020;194(2):570–580. doi:10.1007/s12011-019-01795-3.
  • Ma Y, Zhang Y, Xiao Y, Xiao F. Increased mitochondrial fragmentation mediated by dynamin-related protein 1 contributes to hexavalent chromium-induced mitochondrial respiratory chain complex I-dependent cytotoxicity. Toxics. 2020;8(3):50. doi:10.3390/toxics8030050.
  • Nudler SI, Quinteros FA, Miler EA, et al. Chromium VI administration induces oxidative stress in hypothalamus and anterior pituitary gland from male rats. Toxicol Lett. 2009;185(3):187–192. doi:10.1016/j.toxlet.2009.01.003.
  • Stout MD, Nyska A, Collins BJ, et al. Chronic toxicity and carcinogenicity studies of chromium picolinate monohydrate administered in feed to F344/N rats and B6C3F1 mice for 2 years. Food Chem Toxicol. 2009;47(4):729–733. doi:10.1016/j.fct.2009.01.006.
  • Thompson CM, Proctor DM, Haws LC, et al. Investigation of the mode of action underlying the tumorigenic response induced in B6C3F1 mice exposed orally to hexavalent chromium. Toxicol Sci. 2011;123(1):58–70. doi:10.1093/toxsci/kfr164.
  • Soudani N, Troudi A, Amara IB, et al. Ameliorating effect of selenium on chromium (VI)-induced oxidative damage in the brain of adult rats. J Physiol Biochem. 2012;68(3):397–409. doi:10.1007/s13105-012-0152-4.
  • Samuel JB, Stanley JA, Sekar P, et al. Persistent hexavalent chromium exposure impaired the pubertal development and ovarian histoarchitecture in Wistar rat offspring. Environ Toxicol. 2014;29(7):814–828. doi:10.1002/tox.21810.
  • Suh M, Thompson CM, Kirman CR, et al. High concentrations of hexavalent chromium in drinking water alter iron homeostasis in F344 rats and B6C3F1mice. Food Chem Toxicol. 2014;65(January):381–388. doi:10.1016/j.fct.2014.01.009.
  • Sivakumar KK, Stanley JA, Arosh JA, et al. Prenatal exposure to chromium induces early reproductive senescence by increasing germ cell apoptosis and advancing germ cell cyst breakdown in the f1 offspring. Dev Biol. 2014;388(1):22–34. doi:10.1016/j.ydbio.2014.02.003.
  • Sahu BD, Koneru M, Bijargi SR, et al. Chromium-induced nephrotoxicity and ameliorative effect of carvedilol in rats: involvement of oxidative stress, apoptosis and inflammation. Chem Biol Interact. 2014;223:69–79. doi:10.1016/j.cbi.2014.09.009.
  • Stanley JA, Sivakumar KK, Arosh JA, et al. Edaravone mitigates hexavalent chromium-induced oxidative stress and depletion of antioxidant enzymes while estrogen restores antioxidant enzymes in the rat ovary in f1 offspring1. Biol Reprod. 2014;91(1) doi:10.1095/biolreprod.113.113332.
  • García-Niño WR, Zatarain-Barrón ZL, Hernández-Pando R, et al. Oxidative stress markers and histological analysis in diverse organs from rats treated with a hepatotoxic dose of Cr(VI): effect of curcumin. Biol Trace Elem Res. 2015;167(1):130–145. doi:10.1007/s12011-015-0283-x.
  • Salama A, Hegazy R, Hassan A. Intranasal chromium induces acute brain and lung injuries in rats: assessment of different potential hazardous effects of environmental and occupational exposure to chromium and introduction of a novel pharmacological and toxicological animal model. PLoS One. 2016;11(12):e0168688–e0168688. doi:10.1371/journal.pone.0168688.
  • Abu Zeid EH, Hussein MMA, Ali H. Ascorbic acid protects male rat brain from oral potassium dichromate-induced oxdative DNA damage and apoptotic changes: the expression patterns of caspase-3, p 53, bax, and bcl-2 genes. Environ Sci Pollut Res Int. 2018;25(13):13056–13066. doi:10.1007/s11356-018-1546-9.
  • Zheng W, Ge F, Wu K, et al. In utero exposure to hexavalent chromium disrupts rat fetal testis development. Toxicol Lett. 2018;299:201–209. doi:10.1016/j.toxlet.2018.10.010.
  • Han B, Li S, Lv Y, et al. Dietary melatonin attenuates chromium-induced lung injury: via activating the Sirt1/Pgc-1α/Nrf2 pathway. Food Funct. 2019;10(9):5555–5565. doi:10.1039/c9fo01152h.
  • Zhao Y, Yan J, Li AP, et al. Bone marrow mesenchymal stem cells could reduce the toxic effects of hexavalent chromium on the liver by decreasing endoplasmic reticulum stress-mediated apoptosis via SIRT1/HIF-1α signaling pathway in rats. Toxicol Lett. 2019;310(March):31–38. doi:10.1016/j.toxlet.2019.04.007.
  • Lv Y, Jiang H, Li S, et al. Sulforaphane prevents chromium-induced lung injury in rats via activation of the Akt/GSK-3β/Fyn pathway. Environ Pollut. 2020;259:113812. doi:10.1016/j.envpol.2019.113812.
  • Karaulov AV, Renieri EA, Smolyagin AI, et al. Long-term effects of chromium on morphological and immunological parameters of Wistar rats. Food Chem Toxicol. 2019;133(August):110748. doi:10.1016/j.fct.2019.110748.
  • Thompson CM, Donahue DA, Hobbs C, et al. Exposure to environmentally-relevant concentrations of hexavalent chromium does not induce ovarian toxicity in mice. Regul Toxicol Pharmacol. 2020;116(June):104729. doi:10.1016/j.yrtph.2020.104729.
  • Shobana N, Kumar MK, Navin AK, et al. Prenatal exposure to excess chromium attenuates transcription factors regulating expression of androgen and follicle stimulating hormone receptors in sertoli cells of prepuberal rats. Chem Biol Interact. 2020;328(December)2019:109188. doi:10.1016/j.cbi.2020.109188.
  • Zheng X, Li S, Li J, et al. Hexavalent chromium induces renal apoptosis and autophagy via disordering the balance of mitochondrial dynamics in rats. Ecotoxicol Environ Saf. 2020;204:111061. doi:10.1016/j.ecoenv.2020.111061.
  • Hegazy R, Mansour D, Salama A, et al. Exposure to intranasal chromium triggers dose and time-dependent behavioral and neurotoxicological defects in rats. Ecotoxicol Environ Saf. 2021;216:112220. doi:10.1016/j.ecoenv.2021.112220.
  • Yang D, Yang Q, Fu N, et al. Hexavalent chromium induced heart dysfunction via Sesn2-mediated impairment of mitochondrial function and energy supply. Chemosphere. 2021;264(Pt 2):128547. doi:10.1016/j.chemosphere.2020.128547.
  • Kotyzová D, Hodková A, Bludovská M, Eybl V. Effect of chromium (VI) exposure on antioxidant defense status and trace element homeostasis in acute experiment in rat. Toxicol Ind Health. 2015;31(11):1044–1050. doi:10.1177/0748233713487244.
  • Boşgelmez İİ, Söylemezoğlu T, Güvendik G. The protective and antidotal effects of taurine on hexavalent chromium-induced oxidative stress in mice liver tissue. Biol Trace Elem Res. 2008;125(1):46–58. doi:10.1007/s12011-008-8154-3.
  • Tagliari KC, Vargas VMF, Zimiani K, Cecchini R. Oxidative stress damage in the liver of fish and rats receiving an intraperitoneal injection of hexavalent chromium as evaluated by chemiluminescence. Environ Toxicol Pharmacol. 2004;17(3):149–157. doi:10.1016/j.etap.2004.04.001.
  • Yu X, Yu R-Q, Gui D, et al. Hexavalent chromium induces oxidative stress and mitochondria-mediated apoptosis in isolated skin fibroblasts of Indo-Pacific humpback dolphin. Aquat Toxicol. 2018;203:179–186. doi:10.1016/j.aquatox.2018.08.012.
  • Wise SS, Aboueissa AEM, Martino J, Wise JP. Hexavalent chromium-induced chromosome instability drives permanent and heritable numerical and structural changes and a DNA repair-deficient phenotype. Cancer Res. 2018;78(15):4203–4214. doi:10.1158/0008-5472.CAN-18-0531.
  • Lv Y, Zhang P, Guo J, et al. Melatonin protects mouse spermatogonial stem cells against hexavalent chromium-induced apoptosis and epigenetic histone modification. Toxicol Appl Pharmacol. 2018;340(March)2019:30–38. doi:10.1016/j.taap.2017.12.017.
  • Mehmeti I, Lenzen S, Lortz S. Modulation of Bcl-2-related protein expression in pancreatic beta cells by pro-inflammatory cytokines and its dependence on the antioxidative defense status. Mol Cell Endocrinol. 2011;332(1-2):88–96. doi:10.1016/j.mce.2010.09.017.
  • Redza-Dutordoir M, Averill-Bates DA. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta. 2016;1863(12):2977–2992. doi:10.1016/j.bbamcr.2016.09.012.
  • Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2008;451(7182):1069–1075. doi:10.1038/nature06639.
  • Karaulov AV, Smolyagin AI, Mikhailova IV, et al. Assessment of the combined effects of chromium and benzene on the rat neuroendocrine and immune systems. Environ Res. 2022;207:112096. doi:10.1016/j.envres.2021.112096.
  • Wang X, Son YO, Chang Q, et al. NADPH oxidase activation is required in reactive oxygen species generation and cell transformation induced by hexavalent chromium. Toxicol Sci. 2011;123(2):399–410. doi:10.1093/toxsci/kfr180.
  • Kumar S. Occupational exposure associated with reproductive dysfunction. J Occup Health. 2004;46(1):1–19. doi:10.1539/joh.46.1.
  • Danadevi K, Rozati R, Reddy P, Grover P. Semen quality of Indian welders occupationally exposed to nickel and chromium. Reprod Toxicol. 2003;17(4):451–456. doi:10.1016/S0890-6238(03)00040-6.
  • Navin AK, Aruldhas MM, Navaneethabalakrishnan S, et al. Prenatal exposure to hexavalent chromium disrupts testicular steroidogenic pathway in peripubertal f1 rats. Reprod Toxicol. 2021;101:63–73. doi:10.1016/j.reprotox.2021.01.014.
  • Acharya UR, Mishra M, Mishra I, Tripathy RR. Potential role of vitamins in chromium induced spermatogenesis in Swiss mice. Environ Toxicol Pharmacol. 2004;15(2-3):53–59. doi:10.1016/j.etap.2003.08.010.
  • Das J, Kang MH, Kim E, et al. Hexavalent chromium induces apoptosis in male somatic and spermatogonial stem cells via redox imbalance. Sci Rep. 2015;5(August):13921–13914. doi:10.1038/srep13921.
  • Lv Y, Li T, Yang M, et al. Melatonin attenuates chromium (VI)-induced spermatogonial stem cell/progenitor mitophagy by restoration of METTL3-mediated RNA N6-methyladenosine modification. Front Cell Dev Biol. 2021. 9(June) doi:10.3389/fcell.2021.684398.
  • McKenzie AT, Wang M, Hauberg ME, et al. Brain cell type specific gene expression and co-expression network architectures. Sci Rep. 2018;8(1):1–19. doi:10.1038/s41598-018-27293-5.
  • Zheng W, Aschner M, Ghersi-Egea JF. Brain barrier systems: a new frontier in metal neurotoxicological research. Toxicol Appl Pharmacol. 2003;192(1):1–11. doi:10.1016/S0041-008X(03)00251-5.
  • Haddad-Tóvolli R, Dragano NRV, Ramalho AFS, Velloso LA. Development and function of the blood-brain barrier in the context of metabolic control. Front Neurosci. 2017;11(Apr):224–212. doi:10.3389/fnins.2017.00224.
  • Zheng W, Ghersi-Egea JF. Brain barrier systems play no small roles in toxicant-induced brain disorders. Toxicol Sci. 2020;175(2):147–148. doi:10.1093/toxsci/kfaa053.
  • Sun H, Zhou X, Chen H, et al. Modulation of histone methylation and mlh1 gene silencing by hexavalent chromium. Toxicol Appl Pharmacol. 2009;237(3):258–266. doi:10.1016/j.taap.2009.04.008.
  • Hanson LR, Frey WH. 2nd. Intranasal delivery bypasses the blood-brain barrier to target therapeutic agents to the central nervous system and treat neurodegenerative disease. BMC Neurosci. 2008;9(S3):S5. doi:10.1186/1471-2202-9-S3-S5.
  • Fatima R, Akhtar K, Hossain MM, Ahmad R. Chromium oxide nanoparticle-induced biochemical and histopathological alterations in the kidneys and brain of Wistar rats. Toxicol Ind Health. 2017;33(12):911–921. doi:10.1177/0748233717735266.
  • Stout MD, Herbert RA, Kissling GE, et al. Hexavalent chromium is carcinogenic to F344/N rats and B6C3F1 mice after chronic oral exposure. Environ Health Perspect. 2009;117(5):716–722. doi:10.1289/ehp.0800208.
  • Yatera K, Morimoto Y, Ueno S, et al. Cancer risks of hexavalent chromium in the respiratory tract. J Uoeh. 2018;40(2):157–172. doi:10.7888/juoeh.40.157.
  • Reynolds M, Zhitkovich A. Cellular vitamin C increases chromate toxicity via a death program requiring mismatch repair but not p53. Carcinogenesis. 2007;28(7):1613–1620. doi:10.1093/carcin/bgm031.
  • Peterson-Roth E, Reynolds M, Quievryn G, Zhitkovich A. Mismatch repair proteins are activators of toxic responses to chromium-DNA damage. Mol Cell Biol. 2005;25(9):3596–3607. doi:10.1128/mcb.25.9.3596-3607.2005.
  • Tsuboi M, Kondo K, Soejima S, et al. Chromate exposure induces DNA hypermethylation of the mismatch repair gene MLH1 in lung cancer. Mol Carcinog. 2020;59(1):24–31. doi:10.1002/mc.23125.
  • Wise JP, Young JL, Cai J, Cai L. Current understanding of hexavalent chromium [Cr(VI)] neurotoxicity and new perspectives. Environ Int. 2022;158:106877. doi:10.1016/j.envint.2021.106877.

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