Lead (Pb) induced ATM-dependent mitophagy via PINK1/Parkin pathway

Toxicology Letters

Volumn 291, Issue , 2018, Pages 92-100

  Gu, Xueyan ^a   Qi, Yongmei ^a   Feng, Zengxiu ^a   Ma, Lin ^a   Gao, Ke ^a   Zhang, Yingmei ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

ATM; In vitro; In vivo; Lead; Mitophagy; PINK1 Parkin pathway

Indexed keywords

ATM PROTEIN; LEAD; PARKIN; PHOSPHOTRANSFERASE; PTEN INDUCED PUTATIVE KINASE 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME PHOSPHORYLATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOPHAGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; DRUG EFFECT; GENE KNOCKDOWN; GENETICS; KIDNEY CORTEX; LEAD POISONING; MALE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CYTOSOL; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; KIDNEY CORTEX; LEAD POISONING; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIAL DEGRADATION; PHOSPHORYLATION; PROTEIN KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES;

EID: 85045715967     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2018.04.012     Document Type: Article

References (43)

1. Aerts, L., Craessaerts, K., De Strooper, B., Morais, V.A., PINK1 kinase catalytic activity is regulated by phosphorylation on serines 228 and 402. J. Biol. Chem. 290 (2015), 2798–2811, 10.1074/jbc.M114.620906.
2. Alexander, A., Cai, S.L., Kim, J., Nanez, A., Sahin, M., MacLean, K.H., Inoki, K., Guan, K.L., Shen, J., Person, M.D., Kusewitt, D., Mills, G.B., Kastan, M.B., Walker, C.L., ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 4153–4158, 10.1073/pnas.0913860107.
3. Ambrose, M., Goldstine, J.V., Gatti, R.A., Intrinsic mitochondrial dysfunction in ATM-deficient lymphoblastoid cells. Hum. Mol. Genet. 16 (2007), 2154–2164, 10.1093/hmg/ddm166.
4. Carocci, A., Catalano, A., Lauria, G., Sinicropi, M.S., Genchi, G., Lead toxicity, antioxidant defense and environment. Rev. Environ. Contam. Toxicol. 238 (2016), 45–67, 10.1007/398_2015_5003.
5. Dai, H., Deng, Y., Zhang, J., Han, H., Zhao, M., Li, Y., Zhang, C., Tian, J., Bing, G., Zhao, L., PINK1/Parkin-mediated mitophagy alleviates chlorpyrifos-induced apoptosis in SH-SY5Y cells. Toxicology 334 (2015), 72–80, 10.1016/j.tox.2015.06.003.
6. Derheimer, F.A., Kastan, M.B., Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett. 584 (2010), 3675–3681, 10.1016/j.febslet.2010.05.031.
7. Eiyama, A., Okamoto, K., PINK1/Parkin-mediated mitophagy in mammalian cells. Curr. Opin. Cell Biol. 33 (2015), 95–101, 10.1016/j.ceb.2015.01.002.
8. Goyer, R.A., Krall, R., Ultrastructural transformation in mitochondria isolated from kidneys of normal and lead-intoxicated rats. J. Cell Biol. 41 (1969), 393–400, 10.1083/jcb.41.2.393.
9. Guleria, A., Chandna, S., ATM kinase: much more than a DNA damage responsive protein. DNA Repair 39 (2016), 1–20, 10.1016/j.dnarep.2015.12.009.
10. He, L., Poblenz, A.T., Medrano, C.J., Fox, D.A., Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J. Biol. Chem. 275 (2000), 12175–12184, 10.1074/jbc.275.16.12175.
11. Jin, S.M., Youle, R.J., PINK1- and Parkin-mediated mitophagy at a glance. J. Cell Sci. 125 (2012), 795–799, 10.1242/jcs.093849.
12. Kerr, R.P., Krunkosky, T.M., Hurley, D.J., Cummings, B.S., Holladay, S.D., Gogal, R.M. Jr., Lead at 2.5 and 5.0 (M induced aberrant MH-II surface expression through increased MII exocytosis and increased autophagosome formation in Raw 267.4 cells. Toxicol. In Vitro 27 (2013), 1018–1024, 10.1016/j.tiv.2013.01.018.
13. Khalil, B., El Fissi, N., Aouane, A., Cabirol-Pol, M.J., Rival, T., Lievens, J.C., PINK1-induced mitophagy promotes neuroprotection in Huntington's disease. Cell. Death. Dis., 6, 2015, e1617, 10.1038/cddis.2014.581.
14. Kim, Y., Park, J., Kim, S., Song, S., Kwon, S.K., Lee, S.H., Kitada, T., Kim, J.M., Chung, J., PINK1 controls mitochondrial localization of Parkin through direct phosphorylation. Biochem. Biophys. Res. Commun. 377 (2008), 975–980, 10.1016/j.bbrc.2008.10.104.
15. Kondapalli, C., Kazlauskaite, A., Zhang, N., Woodroof, H.I., Campbell, D.G., Gourlay, R., Burchell, L., Walden, H., Macartney, T.J., Deak, M., Knebel, A., Alessi, D.R., Muqit, M.M., PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol., 2, 2012, 120080, 10.1098/rsob.120080.
16. Li, Z., Liu, X., Wang, L., Wang, Y., Du, C., Xu, S., Zhang, Y., Wang, C., Yang, C., The role of PGC-1alpha and MRP1 in lead-induced mitochondrial toxicity in testicular Sertoli cells. Toxicology 355–356 (2016), 39–48, 10.1016/j.tox.2016.05.016.
17. Liu, J., Jia, D.Y., Cai, S.Z., Li, C.P., Zhang, M.S., Zhang, Y.Y., Yan, C.H., Wang, Y.P., Mitochondria defects are involved in lead-acetate-induced adult hematopoietic stem cell decline. Toxicol. Lett. 235 (2015), 37–44, 10.1016/j.toxlet.2015.03.007.
18. Liu, G., Wang, Z.K., Wang, Z.Y., Yang, D.B., Liu, Z.P., Wang, L., 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 (2016), 1193–1209, 10.1007/s00204-015-1547-0.
19. Lv, X.H., Zhao, D.H., Cai, S.Z., Luo, S.Y., You, T.T., Xu, B.L., Chen, K., Autophagy plays a protective role in cell death of osteoblasts exposure to lead chloride. Toxicol. Lett. 239 (2015), 131–140, 10.1016/j.toxlet.2015.09.014.
20. Matovic, V., Buha, A., Ethukic-Cosic, D., Bulat, Z., Insight into the oxidative stress induced by lead and/or cadmium in blood, liver and kidneys. Food Chem. Toxicol. 78 (2015), 130–140, 10.1016/j.fct.2015.02.011.
21. Narendra, D., Tanaka, A., Suen, D.F., Youle, R.J., Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183 (2008), 795–803, 10.1083/jcb.200809125.
22. Okatsu, K., Oka, T., Iguchi, M., Imamura, K., Kosako, H., Tani, N., Kimura, M., Go, E., Koyano, F., Funayama, M., Shiba-Fukushima, K., Sato, S., Shimizu, H., Fukunaga, Y., Taniguchi, H., Komatsu, M., Hattori, N., Mihara, K., Tanaka, K., Matsuda, N., PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat. Commun., 3, 2012, 1016, 10.1038/ncomms2016.
23. Park, Y.S., Choi, S.E., Koh, H.C., PGAM5 regulates PINK1/Parkin-mediated mitophagy via DRP1 in CCCP-induced mitochondrial dysfunction. Toxicol. Lett. 284 (2018), 120–128, 10.1016/j.toxlet.2017.12.004.
24. Qi, Y.M., Qiu, Q., Gu, X.Y., Tian, Y.H., Zhang, Y.M., ATM mediates spermidine-induced mitophagy via PINK1 and Parkin regulation in human fibroblasts. Sci. Rep., 6, 2016, 24700, 10.1038/srep24700.
25. Shiba-Fukushima, K., Imai, Y., Yoshida, S., Ishihama, Y., Kanao, T., Sato, S., Hattori, N., PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci. Rep., 2, 2012, 1002, 10.1038/srep01002.
26. Song, X.B., Liu, G., Liu, F., Yan, Z.G., Wang, Z.Y., Liu, Z.P., Wang, L., Autophagy blockade and lysosomal membrane permeabilization contribute to lead-induced nephrotoxicity in primary rat proximal tubular cells. Cell. Death. Dis., 8, 2017, e2863, 10.1038/cddis.2017.262.
27. Sui, L., Zhang, R.H., Zhang, P., Yun, K.L., Zhang, H.C., Liu, L., Hu, M.X., Lead toxicity induces autophagy to protect against cell death through mTORC1 pathway in cardiofibroblasts. Biosci. Rep., 2015, 35, 10.1042/bsr20140164.
28. Valentin-Vega, Y.A., Kastan, M.B., A new role for ATM: regulating mitochondrial function and mitophagy. Autophagy 8 (2012), 840–841, 10.4161/auto.19693.
29. Valentin-Vega, Y.A., Maclean, K.H., Tait-Mulder, J., Milasta, S., Steeves, M., Dorsey, F.C., Cleveland, J.L., Green, D.R., Kastan, M.B., Mitochondrial dysfunction in ataxia-telangiectasia. Blood 119 (2012), 1490–1500, 10.1182/blood-2011-08-373639.
30. Wang, L., Li, J.J., Li, J.G., Liu, Z.P., Effects of lead and/or cadmium on the oxidative damage of rat kidney cortex mitochondria. Biol. Trace Elem. Res. 137 (2010), 69–78, 10.1007/s12011-009-8560-1.
31. Wang, Y., Nartiss, Y., Steipe, B., McQuibban, G.A., Kim, P.K., ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 8 (2012), 1462–1476, 10.4161/auto.21211.
32. Wang, Z.K., Zhou, X.L., Song, X.B., Zhuang, D.M., Wang, Z.Y., Yang, D.B., Wang, L., Alleviation of lead-induced apoptosis by puerarin via inhibiting mitochondrial permeability transition pore opening in primary cultures of rat proximal tubular cells. Biol. Trace Elem. Res. 174 (2016), 166–176, 10.1007/s12011-016-0701-8.
33. Wang, B., Nie, J., Wu, L., Hu, Y., Wen, Z., Dong, L., Zou, M.H., Chen, C., Wang, D.W., AMPKalpha2 protects against the development of heart failure by enhancing mitophagy via PINK1 phosphorylation. Circ. Res. 122:5 (2017), 712–729, 10.1161/circresaha.117.312317.
34. Wani, A.L., Ara, A., Usmani, J.A., Lead toxicity: a review. Interdiscip Toxicol 8 (2015), 55–64, 10.1515/intox-2015-0009.
35. Wei, X., Qi, Y., Zhang, X., Gu, X., Cai, H., Yang, J., Zhang, Y., ROS act as an upstream signal to mediate cadmium-induced mitophagy in mouse brain. Neurotoxicology 46 (2015), 19–24, 10.1016/j.neuro.2014.11.007.
36. Wieckowski, M.R., Giorgi, C., Lebiedzinska, M., Duszynski, J., Pinton, P., Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat. Protoc. 4 (2009), 1582–1590, 10.1038/nprot.2009.151.
37. Xiao, B., Deng, X., Lim, G.G.Y., Xie, S., Zhou, Z.D., Lim, K.L., Tan, E.K., Superoxide drives progression of Parkin/PINK1-dependent mitophagy following translocation of Parkin to mitochondria. Cell. Death. Dis., 8, 2017, e3097, 10.1038/cddis.2017.463.
38. Youle, R.J., Narendra, D.P., Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12 (2011), 9–14, 10.1038/nrm3028.
39. Yuan, G., Dai, S., Yin, Z., Lu, H., Jia, R., Xu, J., Song, X., Li, L., Shu, Y., Zhao, X., Chen, Z., Fan, Q., Liang, X., He, C., Yin, L., Lv, C., Lei, Q., Wang, L., Mi, Y., Yu, X., Zhang, M., Sub-chronic lead and cadmium co-induce apoptosis protein expression in liver and kidney of rats. Int. J. Clin. Exp. Pathol. 7 (2014), 2905–2914 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4097244/.
40. Zhang, J.B., Cai, T., Zhao, F., Yao, T., Chen, Y.M., Liu, X.Q., Luo, W.J., Chen, J.Y., The role of alpha-synuclein and tau hyperphosphorylation-mediated autophagy and apoptosis in lead-induced learning and memory injury. Int. J. Biol. Sci. 8 (2012), 935–944, 10.7150/ijbs.4499.
41. Zhang, J., Tripathi, D.N., Jing, J., Alexander, A., Kim, J., Powell, R.T., Dere, R., Tait-Mulder, J., Lee, J.H., Paull, T.T., Pandita, R.K., Charaka, V.K., Pandita, T.K., Kastan, M.B., Walker, C.L., ATM functions at the peroxisome to induce pexophagy in response to ROS. Nat. Cell Biol. 17 (2015), 1259–1269, 10.1038/ncb3230.
42. Zhang, H.T., Mi, L., Wang, T., Yuan, L., Li, X.H., Dong, L.S., Zhao, P., Fu, J.L., Yao, B.Y., Zhou, Z.C., PINK1/Parkin-mediated mitophagy play a protective role in manganese induced apoptosis in SH-SY5Y cells. Toxicol. In Vitro 34 (2016), 212–219, 10.1016/j.tiv.2016.04.006.
43. Zhang, T.M., Xue, L., Li, L., Tang, C.Y., Wan, Z.Q., Wang, R.X., Tan, J.Q., Tan, Y., Han, H.L., Tian, R.Y., Billiar, T.R., Tao, W.A., Zhang, Z.H., BNIP3 protein suppresses PINK1 kinase proteolytic cleavage to promote mitophagy. J. Biol. Chem. 291 (2016), 21616–21629, 10.1074/jbc.M116.733410.