Lead acetate induces apoptosis in Leydig cells by activating PPARγ/caspase-3/PARP pathway

References

• Ai X , Mao F , Shen S , Yang S , Wang J. 2018. Bexarotene inhibits the viability of non-small cell lung cancer cells via slc10a2/PPARγ/PTEN/mTOR signaling pathway. Bmc Cancer. 18(1):407. doi:10.1186/s12885-018-4242-8.
   PubMedGoogle Scholar
• Aksu DS , Sağlam YS , Yildirim S , Aksu T . 2017. Effect of pomegranate (Punica granatum L.) juice on kidney, liver, heart and testis histopathological changes and the tissues lipid peroxidation and antioxidant status in lead acetate-treated rats. Cell Mol Biol. 63(10):33–42. doi:10.14715/cmb/2017.63.10.5.
   PubMed Web of Science ®Google Scholar
• Apostoli P , Kiss P , Porru S , Bonde JP , Vanhoorne M . 1998. Male reproductive toxicity of lead in animals and humans. ASCLEPIOS study group. Occup Environ Med. 55(6):364–374. doi:10.1136/oem.55.6.364.
   PubMed Web of Science ®Google Scholar
• Aquila S , Bonofiglio D , Gentile M , Middea E , Gabriele S , Belmonte M , Catalano S , Pellegrino M , Ando S . 2006. Peroxisome proliferator-activated receptor (PPAR) gamma is expressed by human spermatozoa: its potential role on the sperm physiology. J Cell Physiol. 209(3):977–986. doi:10.1002/jcp.20807.
   PubMed Web of Science ®Google Scholar
• Chi Q , Liu T , Sun Z , Tan S , Li S , Li S . 2017. Involvement of mitochondrial pathway in environmental metal pollutant lead-induced apoptosis of chicken liver: perspectives from oxidative stress and energy metabolism. Environ Sci Pollut Res Int. 24(36):28121–28131. doi:10.1007/s11356-017-0411-6.
   PubMed Web of Science ®Google Scholar
• Fajas L , Egler V , Reiter R , Miard S , Lefebvre AM , Auwerx J . 2003. PPAR gamma controls cell proliferation and apoptosis in an RB-dependent manner. Oncogene. 22(27):4186–4193. doi:10.1038/sj.onc.1206530.
   PubMed Web of Science ®Google Scholar
• Flora SJ , Gautam P , Kushwaha P . 2012. Lead and ethanol co-exposure lead to blood oxidative stress and subsequent neuronal apoptosis in rats. Alcohol Alcohol. 47(2):92–101. doi:10.1093/alcalc/agr152.
   PubMed Web of Science ®Google Scholar
• Gong YG , Wang YQ , Gu M , Feng MM , Zhang W , Ge RS . 2009. Deprival of testicular innervation induces apoptosis of Leydig cells via caspase-8-dependent signaling: a novel survival pathway revealed. Biochem Biophys Res Commun. 382(1):165–170. doi:10.1016/j.bbrc.2009.02.159.
   PubMed Web of Science ®Google Scholar
• Gorowska-Wojtowicz E , Dutka P , Kudrycka M , Pawlicki P , Milon A , Plachno BJ , Tworzydlo W , Pardyak L , Kaminska A , Hejmej A , et al. 2018. Regulation of steroidogenic function of mouse Leydig cells: G-coupled membrane estrogen receptor and peroxisome proliferator-activated receptor partnership. J Physiol Pharmacol. 69(3):373–390.
   Web of Science ®Google Scholar
• Han L , Gao B , Hao H , Zhou H , Lu J , Sun K . 2018. Lead contamination in sediments in the past 20years: A challenge for China. Sci Total Environ. 640–641:746–756. doi:10.1016/j.scitotenv.2018.05.330.
   PubMed Web of Science ®Google Scholar
• He X , Wu J , Yuan L , Lin F , Yi J , Li J , Yuan H , Shi J , Yuan T , Zhang S , et al. 2017. Lead induces apoptosis in mouse TM3 Leydig cells through the Fas/FasL death receptor pathway. Environ Toxicol Pharmacol. 56:99–105. doi:10.1016/j.etap.2017.08.034.
   PubMed Web of Science ®Google Scholar
• Jang MH , Shin MC , Shin HS , Kim KH , Park HJ , Kim EH , Kim CJ . 2002. Alcohol induces apoptosis in TM3 mouse Leydig cells via Bax-dependent caspase-3 activation. Eur J Pharmacol. 449(1–2):39–45.
   PubMed Web of Science ®Google Scholar
• Jin X , Jia T , Liu R , Xu S . 2018. The antagonistic effect of selenium on cadmium-induced apoptosis via PPAR-γ/PI3K/Akt pathway in chicken pancreas. J Hazard Mater. 357:355–362. doi:10.1016/j.jhazmat.2018.06.003.
   PubMed Web of Science ®Google Scholar
• Kasten-Jolly J , Lawrence DA . 2017. Sex-specific effects of developmental lead exposure on the immune-neuroendocrine network. Toxicol Appl Pharmacol. 334:142–157. doi:10.1016/j.taap.2017.09.009.
   PubMed Web of Science ®Google Scholar
• Kota BP , Huang TH , Roufogalis BD . 2005. An overview on biological mechanisms of PPARs. Pharmacol Res. 51(2):85–94. doi:10.1016/j.phrs.2004.07.012.
   PubMed Web of Science ®Google Scholar
• Kushwaha R , Mishra J , Tripathi S , Khare P , Bandyopadhyay S . 2018. Arsenic, cadmium, and lead like troglitazone trigger PPAR gamma-dependent poly (ADP-Ribose) polymerase expression and subsequent apoptosis in rat brain astrocytes. Mol Neurobiol. 55(3):2125–2149. doi:10.1007/s12035-017-0469-7.
   PubMed Web of Science ®Google Scholar
• Li C , Zhao K , Zhang H , Liu L , Xiong F , Wang K , Chen B . 2018. Lead exposure reduces sperm quality and DNA integrity in mice. Environ Toxicol. 33(5):594–602. doi:10.1002/tox.22545.
   PubMed Web of Science ®Google Scholar
• Li Y , Meng Y , Li H , Li J , Fu J , Liu Y , Chen X . 2006. Growth inhibition and differentiation induced by peroxisome proliferator activated receptor gamma ligand rosiglitazone in human melanoma cell line A375. Med Oncol. 23:393–402.
   PubMed Web of Science ®Google Scholar
• Liu G , Wang ZK , Wang ZY , Yang DB , Liu ZP , Wang L . 2016. Mitochondrial permeability transition and its regulatory components are implicated in apoptosis of primary cultures of rat proximal tubular cells exposed to lead. Arch Toxicol. 90(5):1193–1209. doi:10.1007/s00204-015-1547-0.
   PubMed Web of Science ®Google Scholar
• Liu Z , Wang H , Zhang W , Yuan Z , Yuan H , Liu X , Zhang M , Guo X , Guan W . 2018. Lead induces Siberian tiger fibroblast apoptosis by interfering with intracellular homeostasis. Drug Chem Toxicol. 41(2):188–198. doi:10.1080/01480545.2017.1337125.
   PubMed Web of Science ®Google Scholar
• Llop S , Lopez-Espinosa MJ , Rebagliato M , Ballester F . 2013. Gender differences in the neurotoxicity of metals in children. Toxicology. 311(1–2):3–12. doi:10.1016/j.tox.2013.04.015.
   PubMed Web of Science ®Google Scholar
• Luna C , Mendoza N , Casao A , Perez-Pe R , Cebrian-Perez JA , Muino-Blanco T . 2017. c-Jun N-terminal kinase and p38 mitogen-activated protein kinase pathways link capacitation with apoptosis and seminal plasma proteins protect sperm by interfering with both routes. Biol Reprod. 96(4):800–815. doi:10.1093/biolre/iox017.
   PubMed Web of Science ®Google Scholar
• Mao W , Liu J , Fukuoka S , Iwai C , Fu M , Liang C . 2006. Abstract 1284: the calmodulin kinase II (CaMKII)-p38 MAPK-ATF6 pathway is involved in the Endoplasmic Reticulum (ER) stress and Myocyte apoptosis in ß1-Adrenergic Receptor (AR) Peptide induced cardiomyopathy. Circulation. 114(18):II(242).
   Web of Science ®Google Scholar
• McCormack D , McFadden D . 2013. A review of pterostilbene antioxidant activity and disease modification. Oxid Med Cell Longev. 2013:575482. doi:10.1155/2013/575482.
   PubMed Web of Science ®Google Scholar
• Meeker JD , Rossano MG , Protas B , Diamond MP , Puscheck E , Daly D , Paneth N , Wirth JJ . 2008. Cadmium, lead, and other metals in relation to semen quality: human evidence for molybdenum as a male reproductive toxicant. Environ Health Perspect. 116(11):1473–1479. doi:10.1289/ehp.11490.
   PubMed Web of Science ®Google Scholar
• Pant N , Upadhyay G , Pandey S , Mathur N , Saxena DK , Srivastava SP . 2003. Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reprod Toxicol. 17(4):447–450.
   PubMed Web of Science ®Google Scholar
• Porter AG , Janicke RU . 1999. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6(2):99–104. doi:10.1038/sj.cdd.4400476.
   PubMed Web of Science ®Google Scholar
• Ren Y , Sun C , Sun Y , Tan H , Wu Y , Cui B , Wu Z . 2009. PPAR gamma protects cardiomyocytes against oxidative stress and apoptosis via Bcl-2 upregulation. Vascul Pharmacol. 51(2–3):169–174. doi:10.1016/j.vph.2009.06.004.
   PubMed Web of Science ®Google Scholar
• Singh G , Singh V , Sobolewski M , Cory-Slechta DA , Schneider JS . 2018. Sex-dependent effects of developmental lead exposure on the brain. Front Genet. 9:89. doi:10.3389/fgene.2018.00089.
   PubMed Web of Science ®Google Scholar
• Suzuki M , Youle RJ , Tjandra N . 2000. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell. 103(4):645–654.
   PubMed Web of Science ®Google Scholar
• Thoreux-Manlay A , Velez de la Calle JF , Olivier MF , Soufir JC , Masse R , Pinon-Lataillade G . 1995. Impairment of testicular endocrine function after lead intoxication in the adult rat. Toxicology. 100(1–3):101–109.
   PubMed Web of Science ®Google Scholar
• Tsujimoto Y . 1998. Role of Bcl-2 family proteins in apoptosis: apoptosomes or mitochondria? Genes Cells. 3(11):697–707.
   PubMed Web of Science ®Google Scholar
• Varga T , Czimmerer Z , Nagy L . 2011. PPARs are a unique set of fatty acid regulated transcription factors controlling both lipid metabolism and inflammation. Biochim Biophys Acta. 1812(8):1007–1022. doi:10.1016/j.bbadis.2011.02.014.
   PubMed Web of Science ®Google Scholar
• Walensky LD . 2006. BCL-2 in the crosshairs: tipping the balance of life and death. Cell Death Differ. 13(8):1339–1350. doi:10.1038/sj.cdd.4401992.
   PubMed Web of Science ®Google Scholar
• Walker WH . 2011. Testosterone signaling and the regulation of spermatogenesis. Spermatogenesis. 1(2):116–120. doi:10.4161/spmg.1.2.16956.
   PubMedGoogle Scholar
• Wang H , Zhai N , Chen Y , Xu H , Huang K . 2017. Cadmium induces Ca 2+ mediated, calpain-1/caspase-3-dependent apoptosis in primary cultured rat proximal tubular cells. J Inorg Biochem. 172:16–22. doi:10.1016/j.jinorgbio.2017.04.005.
   PubMed Web of Science ®Google Scholar
• Wang J , Lv X , Shi J , Hu X , Du Y . 2011. Troglitazone induced apoptosis via PPAR gamma activated POX-induced ROS formation in HT29 cells. Biomed Environ Sci. 24(4):391–399. doi:10.3967/0895-3988.2011.04.010.
   PubMed Web of Science ®Google Scholar
• Wang X , An Y , Jiao W , Zhang Z , Han H , Gu X , Teng X . 2018. Selenium protects against lead-induced apoptosis via endoplasmic reticulum stress in chicken kidneys. Biol Trace Elem Res. 182(2):354–363. doi:10.1007/s12011-017-1097-9.
   PubMed Web of Science ®Google Scholar
• Wang Y , Fang J , Huang S , Chen L , Fan G , Wang C . 2013. The chronic effects of low lead level on the expressions of Nrf2 and Mrp1 of the testes in the rats. Environ Toxicol Pharmacol. 35(1):109–116. doi:10.1016/j.etap.2012.12.001.
   PubMed Web of Science ®Google Scholar
• Wirth JJ , Mijal RS . 2010. Adverse effects of low level heavy metal exposure on male reproductive function. Syst Biol Reprod Med. 56(2):147–167. doi:10.3109/19396360903582216.
   PubMed Web of Science ®Google Scholar
• Wu HY , Yang F , Li HP , Li QB , Zhang FL , Ba Y , Cui LX , Sun LL , Lv TC , Wang N , et al. 2019. Heavy metal pollution and health risk assessment of agricultural soil near a smelter in an industrial city in China. Int J Environ Health Res. 1–13. doi:10.1080/09603123.2019.1584666.
   PubMed Web of Science ®Google Scholar
• Yang WY , Zhang ZY , Thijs L , Cauwenberghs N , Wei FF , Jacobs L , Luttun A , Verhamme P , Kuznetsova T , Nawrot TS , et al. 2017. Left ventricular structure and function in relation to environmental exposure to lead and cadmium. J Am Heart Assoc. 6(2):e004692. doi:10.1161/JAHA.116.004692.
   PubMed Web of Science ®Google Scholar
• Yedjou CG , Tchounwou HM , Tchounwou PB . 2015. DNA damage, cell cycle arrest, and apoptosis induction caused by lead in human leukemia cells. Int J Environ Res Public Health. 13(1):ijerph13010056. doi:10.3390/ijerph13010035.
   PubMed Web of Science ®Google Scholar
• Zander T , Kraus JA , Grommes C , Schlegel U , Feinstein D , Klockgether T , Landreth G , Koenigsknecht J , Heneka MT . 2002. Induction of apoptosis in human and rat glioma by agonists of the nuclear receptor PPARγ. J Neurochem. 81:1052–1060.
   PubMed Web of Science ®Google Scholar
• Zhao D , Zhang X . 2018. Selenium antagonizes the lead-induced apoptosis of chicken splenic lymphocytes in vitro by activating the PI3K/Akt pathway. Biol Trace Elem Res. 182(1):119–129. doi:10.1007/s12011-017-1088-x.
   PubMed Web of Science ®Google Scholar