Role of autophagy in methylmercury-induced neurotoxicity in rat primary astrocytes

Archives of Toxicology

Volumn 90, Issue 2, 2016, Pages 333-345

  Yuntao, Fang ^a   Chenjia, Guo ^a   Panpan, Zhang ^a   Wenjun, Zhao ^a   Suhua, Wang ^a   Guangwei, Xing ^a   Haifeng, Shi ^a   Jian, Lu ^a   Wanxin, Peng ^a   Yun, Feng ^a   Cai, Jiyang ^b   Aschner, Michael ^c   Rongzhu, Lu ^a  

^a JIANGSU UNIVERSITY   (China)

^b University of Texas Medical Branch School of Medicine   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Antioxidants; Astrocytes; Autophagy; Methylmercury; Neuroprotection; Neurotoxicity

Indexed keywords

3 METHYLADENINE; ACETYLCYSTEINE; AUTOPHAGY PROTEIN 5; BECLIN 1; CASPASE 3; CHLOROQUINE; METHYLMERCURY; PROTEIN P62; RAPAMYCIN; SMALL INTERFERING RNA; ATG5 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN 5; METHYLMERCURY DERIVATIVE;

ANALYSIS; ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; AUTOPHAGY; CELL VIABILITY; CONTROLLED STUDY; GENE SILENCING; MTT ASSAY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; ANIMAL; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; GENETICS; METABOLISM; NEUROTOXICITY SYNDROMES; PATHOLOGY;

ACETYLCYSTEINE; ANIMALS; APOPTOSIS; ASTROCYTES; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 5; CELLS, CULTURED; CHLOROQUINE; DOSE-RESPONSE RELATIONSHIP, DRUG; METHYLMERCURY COMPOUNDS; NEUROTOXICITY SYNDROMES; RATS;

EID: 84958119341     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1425-1     Document Type: Article

References (78)

1. Aki T, Funakoshi T, Unuma K, Uemura K (2013) Impairment of autophagy: from hereditary disorder to drug intoxication. Toxicology 311(3):205–215. doi:10.1016/j.tox.2013.07.001
2. 3H-d-aspartate transport in cultured astrocytes is reversed by the antioxidant catalase. Brain Res 902(1):92–100. doi:10.1016/S0006-8993(01)02375-7
3. Allen JW, Shanker G, Tan KH, Aschner M (2002) The consequences of methylmercury exposure on interactive functions between astrocytes and neurons. Neurotoxicology 23(6):755–759. doi:10.1016/S0161-813X(01)00076-6
4. Aschner M (2012) Considerations on methylmercury (MeHg) treatments in in vitro studies. Neurotoxicology 33(3):512–513. doi:10.1016/j.neuro.2012.05.002
5. Aschner M, Du YL, Gannon M, Kimelberg HK (1993) Methylmercury-induced alterations in excitatory amino acid transport in rat primary astrocyte cultures. Brain Res 602(2):181–186. doi:10.1016/0006-8993(93)90680-L
6. Aschner M, Yao CP, Allen JW, Tan KH (2000) Methylmercury alters glutamate transport in astrocytes. Neurochem Int 37(2–3):199–206. doi:10.1016/S0197-0186(00)00023-1
7. Ballatori N, Lieberman MW, Wang W (1998) N-Acetylcysteine as an antidote in methylmercury poisoning. Environ Health Perspect 106(5):267–271. doi:10.1289/ehp.98106267
8. Bitto A, Lerner CA, Nacarelli T, Crowe E, Torres C, Sell C (2014) p62/SQSTM1 at the interface of aging, autophagy, and disease. Age (Dordr) 36(3):9626. doi:10.1007/s11357-014-9626-3
9. Castoldi AF, Coccini T, Ceccatelli S, Manzo L (2001) Neurotoxicity and molecular effects of methylmercury. Brain Res Bull 55(2):197–203. doi:10.1016/S0361-9230(01)00458-0
10. Chang JW, Choi H, Cotman SL, Jung YK (2011) Lithium rescues the impaired autophagy process in CbCln3(∆ex7/8/∆ex7/8) cerebellar cells and reduces neuronal vulnerability to cell death via IMPase inhibition. J Neurochem 116(4):659–668. doi:10.1111/j.1471-4159.2010.07158.x
11. Chang SH, Lee HJ, Kang B et al (2013) Methylmercury induces caspase-dependent apoptosis and autophagy in human neural stem cells. J Toxicol Sci 38(6):823–831. doi:10.1016/j.tiv.2014.09.006
12. Chargui A, Zekri S, Jacquillet G et al (2011) Cadmium-induced autophagy in rat kidney: an early biomarker of subtoxic exposure. Toxicol Sci 121(1):31–42. doi:10.1093/toxsci/kfr031kfr031
13. Chatterjee S, Ray A, Mukherjee S, Agarwal S, Kundu R, Bhattacharya S (2012) Low concentration of mercury induces autophagic cell death in rat hepatocytes. Toxicol Ind Health 30(7):611–620. doi:10.1177/0748233712462442
14. Chatterjee S, Nandi P, Mukherjee S, Chattopadhyay A, Bhattacharya S (2013) Regulation of autophagy in rat hepatocytes treated in vitro with low concentration of mercury. Toxicol Environ Chem 95(3):504–514. doi:10.1080/02772248.2013.786941
15. Chen Y, Gibson SB (2008) Is mitochondrial generation of reactive oxygen species a trigger for autophagy? Autophagy 4(2):246–248. doi:10.4161/auto.5432
16. Chen Z, Fu Q, Shen B, Huang X, Wang K, He P, Li F, Zhang F, Shen H (2014) Enhanced p62 expression triggers concomitant autophagy and apoptosis in a rat chronic spinal cord compression model. Mol Med Rep 9(6):2091–2096. doi:10.3892/mmr.2014.2124
17. Cherra SJ 3rd, Dagda RK, Chu CT (2010) Review: autophagy and neurodegeneration: survival at a cost? Neuropathol Appl Neurobiol 36(2):125–132. doi:10.1111/j.1365-2990.2010.01062.xNAN1062
18. Choi BH (1989) The effects of methylmercury on the developing brain. Prog Neurobiol 32(6):447–470. doi:10.1016/j.annepidem.2005.06.059
19. Choi BH, Lapham LW, Amin-Zaki L, Saleem T (1978) Abnormal neuronal migration, deranged cerebral cortical organization, and diffuse white matter astrocytosis of human fetal brain: a major effect of methylmercury poisoning in utero. J Neuropathol Exp Neurol 37(6):719–733
20. Cuervo AM, Bergamini E, Brunk UT, Droge W, Ffrench M, Terman A (2005) Autophagy and aging: the importance of maintaining “clean” cells. Autophagy 1(3):131–140. doi:10.4161/auto.1.3.2017
21. Cui Q, Tashiro S, Onodera S, Minami M, Ikejima T (2007) Autophagy preceded apoptosis in oridonin-treated human breast cancer MCF-7 cells. Biol Pharm Bull 30(5):859–864. doi:10.1248/bpb.30.859
22. Daré E, Li W, Zhivotovsky B, Yuan X, Ceccatelli S (2001) Methylmercury and H(2)O(2) provoke lysosomal damage in human astrocytoma D384 cells followed by apoptosis. Free Radic Biol Med 30(12):1347–1356. doi:10.1016/S0891-5849(01)00526-3
23. Deng Y, Xu Z, Xu B et al (2014) Exploring cross-talk between oxidative damage and excitotoxicity and the effects of riluzole in the rat cortex after exposure to methylmercury. Neurotox Res 26(1):40–51. doi:10.1007/s12640-013-9448-6
24. Dong Z, Wang L, Xu J et al (2009) Promotion of autophagy and inhibition of apoptosis by low concentrations of cadmium in vascular endothelial cells. Toxicol In Vitro 23(1):105–110. doi:10.1016/j.tiv.2008.11.003
25. Dreiem A, Seegal RF (2007) Methylmercury-induced changes in mitochondrial function in striatal synaptosomes are calcium-dependent and ROS-independent. Neurotoxicology 28(4):720–726. doi:10.1016/j.neuro.2007.03.004
26. Duan WJ, Liu FL, He RR et al (2013) Autophagy is involved in the effects of resveratrol on prevention of splenocyte apoptosis caused by oxidative stress in restrained mice. Mol Nutr Food Res 57(7):1145–1157. doi:10.1002/mnfr.201200662
27. Essick EE, Sam F (2010) Oxidative stress and autophagy in cardiac disease, neurological disorders, aging and cancer. Oxid Med Cell Longev 3(3):168–177. doi:10.4161/oxim.3.3.1210612106
28. Farina M, Rocha JB, Aschner M (2011a) Mechanisms of methylmercury-induced neurotoxicity: evidence from experimental studies. Life Sci 89(15–16):555–563. doi:10.1016/j.lfs.2011.05.019S0024-3205(11)00265-7
29. Farina M, Aschner M, Rocha JB (2011b) Oxidative stress in MeHg-induced neurotoxicity. Toxicol Appl Pharmacol 256(3):405–417. doi:10.1016/j.taap.2011.05.001
30. Fu H, Dou J, Li W et al (2008) Mecamylamine prevents neuronal apoptosis induced by glutamate and low potassium via differential anticholinergic-independent mechanisms. Neuropharmacology 54(4):755–765. doi:10.1016/j.neuropharm.2007.12.003
31. Galavotti S, Bartesaghi S, Faccenda D et al (2013) The autophagy-associated factors DRAM1 and p62 regulate cell migration and invasion in glioblastoma stem cells. Oncogene 32(6):699–712. doi:10.1038/onc.2012.111
32. Guo WJ, Ye SS, Cao N, Huang J, Gao J, Chen QY (2010) ROS-mediated autophagy was involved in cancer cell death induced by novel copper(II) complex. Exp Toxicol Pathol 62(5):577–582. doi:10.1016/j.etp.2009.08.001
33. Harhaji-Trajkovic L, Vilimanovich U, Kravic-Stevovic T, Bumbasirevic V, Trajkovic V (2009) AMPK-mediated autophagy inhibits apoptosis in cisplatin-treated tumour cells. J Cell Mol Med 13(9B):3644–3654. doi:10.1111/j.1582-4934.2009.00663.x
34. Hong MY, Gao JL, Cui JZ et al (2012a) Effect of c-Jun NH(2)-terminal kinase-mediated p53 expression on neuron autophagy following traumatic brain injury in rats. Chin Med J (Engl) 125(11):2019–2024. doi:10.3760/cma.j.issn.0366-6999.2012.11.032
35. Hong YS, Hunter S, Clayton LA, Rifkin E, Bouwer EJ (2012b) Assessment of mercury and selenium concentrations in captive bottlenose dolphin’s (Tursiops truncatus) diet fish, blood, and tissue. Sci Total Environ 414:220–226. doi:10.1016/j.scitotenv.2011.11
36. Jain A, Lamark T, Sjøttem E et al (2010) p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem 285(29):22576–22591. doi:10.1074/jbc.M110.118976
37. Jones SA, Mills KH, Harris J (2013) Autophagy and inflammatory diseases. Immunol Cell Biol 91(3):250–258. doi:10.1038/icb.2012.82icb201282
38. Kroemer G, Levine B (2008) Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 9(12):1004–1010. doi:10.1038/nrm2529nrm2529
39. Laha D, Pramanik A, Maity J et al (2014) Interplay between autophagy and apoptosis mediated by copper oxide nanoparticles in human breast cancer cells MCF7. Biochim Biophys Acta 1840(1):1–9. doi:10.1016/j.bbagen.2013.08.011
40. Larsen KE, Sulzer D (2002) Autophagy in neurons: a review. Histol Histopathol 17(3):897–908
41. Larsen KB, Lamark T, Overvatn A, Harneshaug I, Johansen T, Bjorkoy G (2010) A reporter cell system to monitor autophagy based on p62/SQSTM1. Autophagy 6(6):784–793. doi:10.4161/auto.6.6.12510
42. Liou JS, Wu YC, Yen WY et al (2014) Inhibition of autophagy enhances DNA damage-induced apoptosis by disrupting CHK1-dependent S phase arrest. Toxicol Appl Pharmacol. doi:10.1016/j.taap.2014.04.028
43. Liu AJ, Wang SH, Chen KC et al (2013a) Evodiamine, a plant alkaloid, induces calcium/JNK-mediated autophagy and calcium/mitochondria-mediated apoptosis in human glioblastoma cells. Chem Biol Interact 205(1):20–28. doi:10.1016/j.cbi.2013.06.004
44. Liu W, Xu Z, Deng Y, Xu B, Wei Y, Yang T (2013b) Protective effects of memantine against methylmercury-induced glutamate dyshomeostasis and oxidative stress in rat cerebral cortex. Neurotox Res 24(3):320–337. doi:10.1007/s12640-013-9386-3
45. Liu W, Xu Z, Deng Y et al (2014) Excitotoxicity and oxidative damages induced by methylmercury in rat cerebral cortex and the protective effects of tea polyphenols. Environ Toxicol 29(3):269–283. doi:10.1002/tox.21755
46. Mader BJ, Pivtoraiko VN, Flippo HM et al (2012) Rotenone inhibits autophagic flux prior to inducing cell death. ACS Chem Neurosci 3(12):1063–1072. doi:10.1021/cn300145z
47. Milisav I, Poljsak B, Suput D (2012) Adaptive response, evidence of cross-resistance and its potential clinical use. Int J Mol Sci 13(9):10771–10806. doi:10.3390/ijms130910771ijms-13-10771
48. Ni M, Li X, Rocha JB, Farina M, Aschner M (2012) Glia and methylmercury neurotoxicity. J Toxicol Environ Health A 75(16–17):1091–1101. doi:10.1080/15287394.2012.697840
49. Orrenius S, Kaminskyy VO, Zhivotovsky B (2013) Autophagy in toxicology: cause or consequence? Annu Rev Pharmacol Toxicol 53:275–297. doi:10.1146/annurev-pharmtox-011112-140210
50. Palmeira-Dos-Santos C, Pereira GJ, Barbosa CM, Jurkiewicz A, Smaili SS, Bincoletto C (2014) Comparative study of autophagy inhibition by 3MA and CQ on Cytarabine-induced death of leukaemia cells. J Cancer Res Clin Oncol. doi:10.1007/s00432-014-1640-4
51. Pourahmad J, O’Brien PJ (2001) Biological reactive intermediates that mediate chromium (VI) toxicity. In: Dansette PM, Snyder R, Delaforge M et al (eds) Biological reactive intermediates VI. Springer, Berlin, pp 203–207
52. Puissant A, Auberger P (2010) AMPK- and p62/SQSTM1-dependent autophagy mediate resveratrol-induced cell death in chronic myelogenous leukemia. Autophagy 6(5):655–657. doi:10.4161/auto.6.5.12126
53. Rami A (2009) Review: autophagy in neurodegeneration: firefighter and/or incendiarist? Neuropathol Appl Neurobiol 35(5):449–461. doi:10.1111/j.1365-2990.2009.01034.xNAN1034
54. Ranjan K, Sharma A, Surolia A, Pathak C (2014) Regulation of HA14-1 mediated oxidative stress, toxic response, and autophagy by curcumin to enhance apoptotic activity in human embryonic kidney cells. BioFactors 40(1):157–169. doi:10.1002/biof.1098
55. Sanfeliu C, Sebastia J, Ki SU (2001) Methylmercury neurotoxicity in cultures of human neurons, astrocytes, neuroblastoma cells. Neurotoxicology 22(3):317–327. doi:10.1016/S0161813X01000158
56. Seto S, Tsujimura K, Horii T, Koide Y (2013) Autophagy adaptor protein p62/SQSTM1 and autophagy-related gene Atg5 mediate autophagosome formation in response to Mycobacterium tuberculosis infection in dendritic cells. PLoS One 8(12):e86017. doi:10.1371/journal.pone.0086017PONE-D-13-43593
57. Shanker G, Aschner M (2001) Identification and characterization of uptake systems for cystine and cysteine in cultured astrocytes and neurons: evidence for methylmercury-targeted disruption of astrocyte transport. J Neurosci Res 66(5):998–1002. doi:10.1002/jnr.10066
58. Shanker G, Aschner M (2003) Methylmercury-induced reactive oxygen species formation in neonatal cerebral astrocytic cultures is attenuated by antioxidants. Brain Res Mol Brain Res 110(1):85–91. doi:10.1016/j.neuro.2012.03.004
59. Shanker G, Allen JW, Mutkus LA, Aschner M (2001) Methylmercury inhibits cysteine uptake in cultured primary astrocytes, but not in neurons. Brain Res 914(1–2):159–165. doi:10.1016/S0006-8993(01)02791-3
60. Shapiro AM, Chan HM (2008) Characterization of demethylation of methylmercury in cultured astrocytes. Chemosphere 74(1):112–118. doi:10.1016/j.chemosphere.2008.09.019
61. Shen S, Kepp O, Kroemer G (2012) The end of autophagic cell death? Autophagy 8(1):1–3. doi:10.4161/auto.8.1.1661816618
62. Son YO, Wang X, Hitron JA et al (2011) Cadmium induces autophagy through ROS-dependent activation of the LKB1-AMPK signaling in skin epidermal cells. Toxicol Appl Pharmacol 255(3):287–296. doi:10.1016/j.taap.2011.06.024S0041-008X(11)00257-2
63. Takeuchi T (1985) Human effects of methylmercury as an environmental neurotoxicant. In: Blum K, Manzo L (eds) Neurotoxicology. Marcel Dekker, New York, pp 345–367
64. Tamm C, Duckworth J, Hermanson O, Ceccatelli S (2006) High susceptibility of neural stem cells to methylmercury toxicity: effects on cell survival and neuronal differentiation. J Neurochem 97(1):69–78. doi:10.1111/j.1471-4159.2006.03718.x
65. Tasdemir E, Galluzzi L, Maiuri MC et al (2008) Methods for assessing autophagy and autophagic cell death. Methods Mol Biol 445:29–76. doi:10.1007/978-1-59745-157-4-3
66. Thoreen CC, Sabatini DM (2009) Rapamycin inhibits mTORC1, but not completely. Autophagy 5(5):725–726. doi:10.4161/auto.5.5.8504
67. Tofighi R, Johansson C, Goldoni M et al (2011) Hippocampal neurons exposed to the environmental contaminants methylmercury and polychlorinated biphenyls undergo cell death via parallel activation of calpains and lysosomal proteases. Neurotox Res 19(1):183–194. doi:10.1007/s12640-010-9159-1
68. Wagner C, Vargas AP, Roos DH et al (2010) Comparative study of quercetin and its two glycoside derivatives quercitrin and rutin against methylmercury (MeHg)-induced ROS production in rat brain slices. Arch Toxicol 84(2):89–97. doi:10.1007/s00204-009-0482-3
69. Wang L, Cano M, Handa JT (2014) p62 provides dual cytoprotection against oxidative stress in the retinal pigment epithelium. Biochim Biophys Acta 1843(7):1248–1258. doi:10.1016/j.bbamcr.2014.03.016
70. Wang SH, Shih YL, Kuo TC, Ko WC, Shih CM (2009) Cadmium toxicity toward autophagy through ROS-activated GSK-3beta in mesangial cells. Toxicol Sci 108(1):124–131. doi:10.1093/toxsci/kfn266kfn266
71. Wang Q, Zhu J, Zhang K et al (2013) Induction of cytoprotective autophagy in PC-12 cells by cadmium. Biochem Biophys Res Commun 438(1):186–192. doi:10.1016/j.bbrc.2013.07.050S0006-291X(13)01201-1
72. Wei M, Duan D, Liu Y, Wang Z, Li Z (2014) Autophagy may protect MC3T3-E1 cells from fluoride-induced apoptosis. Mol Med Rep 9(6):2309–2315. doi:10.3892/mmr.2014.2079
73. Wormser U, Brodsky B, Milatovic D et al (2012) Protective effect of a novel peptide against methylmercury-induced toxicity in rat primary astrocytes. Neurotoxicology 33(4):763–768. doi:10.1016/j.neuro.2011.12.004S0161-813X(11)00213-0
74. Wu Y, Wang X, Guo H et al (2013) Synthesis and screening of 3-MA derivatives for autophagy inhibitors. Autophagy 9(4):595–603. doi:10.4161/auto.2364123641
75. Yang L, Hu N, Jiang S et al (2014) Heavy metal scavenger metallothionein attenuates ER stress-induced myocardial contractile anomalies: role of autophagy. Toxicol Lett 225(3):333–341. doi:10.1016/j.toxlet.2013.12.024
76. Yin Z, Lee E, Ni M et al (2011) Methylmercury-induced alterations in astrocyte functions are attenuated by ebselen. Neurotoxicology 32(3):291–299. doi:10.1016/j.neuro.2011.01.004
77. Zhang Q, Yang YJ, Wang H et al (2012) Autophagy activation: a novel mechanism of atorvastatin to protect mesenchymal stem cells from hypoxia and serum deprivation via AMP-activated protein kinase/mammalian target of rapamycin pathway. Stem Cells Dev 21(8):1321–1332. doi:10.1089/scd.2011.0684
78. Zhang YB, Gong JL, Xing TY, Zheng SP, Ding W (2013) Autophagy protein p62/SQSTM1 is involved in HAMLET-induced cell death by modulating apoptosis in U87MG cells. Cell Death Dis 4:e550. doi:10.1038/cddis.2013.77cddis201377