Melatonin Ameliorates Arsenite-Induced Neurotoxicity: Involvement of Autophagy and Mitochondria

Molecular Neurobiology

Volumn 52, Issue 2, 2015, Pages 1015-1022

  Teng, Y C ^a   Tai, Y I ^a   Huang, H J ^b   Lin, A M Y ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

Arsenite; Autophagy; Melatonin; Mitochondria; synuclein

Indexed keywords

3 METHYLADENINE; ALPHA SYNUCLEIN; ARSENIC TRIOXIDE; BIOLOGICAL MARKER; CYTOCHROME C; FLUORESCENT DYE; MELATONIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; NEUROMODULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; UNCLASSIFIED DRUG; 3-METHYLADENINE; ADENINE; ANTIOXIDANT; ARSENITE SODIUM; ARSENOUS ACID DERIVATIVE; CYTOCHROME C OXIDASE; NERVE PROTEIN; NEUROPROTECTIVE AGENT; PPARGC1A PROTEIN, RAT; SODIUM DERIVATIVE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOLYSOSOME; AUTOPHAGY; BIOGENESIS; BRAIN CORTEX; CELL LOSS; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; FEMALE; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; MITOCHONDRION; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PROTEIN LOCALIZATION; RAT; STAINING; ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; LYSOSOME; METABOLISM; PHYSIOLOGY; PREGNANCY; SPRAGUE DAWLEY RAT;

ADENINE; ALPHA-SYNUCLEIN; ANIMALS; ANTIOXIDANTS; ARSENITES; AUTOPHAGY; BIOMARKERS; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT COMPLEX IV; FEMALE; LYSOSOMES; MELATONIN; MITOCHONDRIA; NERVE TISSUE PROTEINS; NEURONS; NEUROPROTECTIVE AGENTS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SODIUM COMPOUNDS; TRANSCRIPTION FACTORS;

EID: 84940796832     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9250-y     Document Type: Article

References (52)

1. Danan M, Dally S, Conso F (1984) Arsenic-induced encephalopathy. Neurology 34:15–24
2. Bolla-Wilson K, Bleecker ML (1987) Neuropsychological impairment following inorganic arsenic exposure. J Occup Med 29:500–503
3. Tyler CR, Allan AM (2014) The effects of arsenic exposure on neurological and cognitive dysfunction in human and rodent studies: a review. Curr Environ Health Rep 1:132–147
4. Grandjean P, Herz KT (2014) Trace elements as paradigms of developmental neurotoxicants: lead, methylmercury and arsenic. J Trace Elem Med Biol. doi:10.1016/j.jtemb
5. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87
6. Bernstam L, Nriagu J (2000) Molecular aspects of arsenic stress. J Toxicol Environ Health B Crit Rev 3:293–322
7. Bashir S, Sharma Y, Irshad M, Gupta SD, Dogra TD (2006) Arsenic-induced cell death in liver and brain of experimental rats. Basic Clin Pharmacol Toxicol 98:38–43
8. Lu TH, Tseng TJ, Su CC, Tang FC, Yen CC, Liu YY, Yang CY, Wu CC et al (2014) Arsenic induces reactive oxygen species-caused neuronal cell apoptosis through JNK/ERK-mediated mitochondria-dependent and GRP 78/CHOP-regulated pathways. Toxicol Lett 224:130–140
9. Piao F, Ma N, Hiraku Y, Murata M, Oikawa S, Cheng F, Zhong L, Yamauchi T et al (2005) Oxidative DNA damage in relation to neurotoxicity in the brain of mice exposed to arsenic at environmentally relevant levels. J Occup Health 47:445–449
10. Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes CJ, Valko M (2011) Arsenic: toxicity, oxidative stress and human disease. J Appl Toxicol 31:95–107
11. Flora SJ (2011) Arsenic-induced oxidative stress and its reversibility. Free Radic Biol Med 51:257–281
12. Dwivedi N, Mehta A, Yadav A, Binukumar BK, Gill KD, Flora SJ (2011) MiADMSA reverses impaired mitochondrial energy metabolism and neuronal apoptotic cell death after arsenic exposure in rats. Toxicol Appl Pharmacol 256:241–248
13. Chattopadhyay S, Bhaumik S, Purkayastha M, Basu S, Nag Chaudhuri A, Das Gupta S (2002) Apoptosis and necrosis in developing brain cells due to arsenic toxicity and protection with antioxidants. Toxicol Lett 6:665–676
14. Chao PL, Fan SF, Chou YH, Lin AMY (2010) N-acetylcysteine attenuates arsenite-induced oxidative injury in DRG explants. Ann N Y Acad Sci 1122:276–288
15. Teng YC, Tai YI, Lee YH, Lin AM (2013) Role of HO-1 in the arsenite-induced neurotoxicity in primary cultured cortical neurons. Mol Neurobiol 48:281–287
16. Yadav RS, Sankhwar ML, Shukla RK, Chandra R, Pant AB, Islam F, Khanna VK (2009) Attenuation of arsenic neurotoxicity by curcumin in rats. Toxicol Appl Pharmacol 240:367–376
17. Galano A, Tan DX, Reiter RJ (2011) Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 51:1–16
18. Romero A, Ramos E, de Los RC, Egea J, Del Pino J, Reiter RJ (2014) A review of metal-catalyzed molecular damage: protection by melatonin. J Pineal Res 56:343–370
19. Pal S, Chatterjee AK (2006) Possible beneficial effects of melatonin supplementation on arsenic-induced oxidative stress in Wistar rats. Drug Chem Toxicol 29:423–433
20. Lin AMY, Fang SF, Chao PL, Yang CH (2007) Melatonin attenuates arsenite-induced apoptosis in rat brain: involvement of mitochondrial and ER pathways and aggregation of α-synuclein. J Pineal Res 43:163–171
21. Lin AM, Feng SF, Chao PL, Yang CH (2009) Melatonin inhibits arsenite-induced peripheral neurotoxicity. J Pineal Res 46:64–70
22. Reiter RJ, Tan DX, Rosales-Corral S, Manchester LC (2013) The universal nature, unequal distribution and antioxidant functions of melatonin and its derivatives. Mini Rev Med Chem 13:373–384
23. Bursch W, Ellinger A, Gerner C, Frohwein U, Schulte-Hermann R (2000) Programmed cell death (PCD): apoptosis autophagic PCD or others? Ann N Y Acad Sci 926:1–12
24. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290:1717–1721
25. Levine B (2003) Autophagy in development, tumor suppression, and innate immunity. Harvey Lect 99:47–76
26. Uchiyama Y, Shibata M, Koike M, Yoshimura K, Sasaki M (2008) Autophagy-physiology and pathophysiology. Histochem Cell Biol 129:407–420
27. Cuervo AM (2004) Autophagy: in sickness and in health. Trends Cell Biol 14:70–77
28. +-induced neurotoxicity in SH-SY5Y cells. Free Radic Biol Med 49:839–846
29. Viscomi MT, D’Amelio M, Cavallucci V, Latini L, Bisicchia E, Nazio F, Fanelli F, Maccarrone M et al (2012) Stimulation of autophagy by rapamycin protects neurons from remote degeneration after acute focal brain damage. Autophagy 8:222–235
30. Zhu JH, Horbinski C, Guo F, Watkins S, Uchiyama Y, Chu CT (2000) Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am J Pathol 170:75–86
31. Chang CF, Huang HJ, Lee HC, Hung KC, Wu RT, Lin AM (2012) Melatonin attenuates kainic acid-induced neurotoxicity in mouse hippocampus via inhibition of autophagy and α-synuclein aggregation. J Pineal Res 52:312–321
32. Cheng TJ, Wang YJ, Kao WW, Chen RJ, Ho YS (2007) Protection against arsenic trioxide-induced autophagic cell death in U118 human glioma cells by use of lipoic acid. Food Chem Toxicol 45:1027–1038
33. Teng YC, Jeng CJ, Huang HJ, Lin AMY (2015) Role of autophagy in arsenite-induced neurotoxicity: the involvement of α-synuclein. Toxicol Lett 233(3):239–45
34. Kubli DA, Gustafsson ÅB (2012) Mitochondria and mitophagy: the yin and yang of cell death control. Circ Res 111:1208–1221
35. Xilouri M, Vogiatzi T, Vekrellis K, Stefanis L (2008) Alpha-synuclein degradation by autophagic pathways: a potential key to Parkinson’s disease pathogenesis. Autophagy 4:917–919
36. Cheng F, Vivacqua G, Yu S (2011) The role of α-synuclein in neurotransmission and synaptic plasticity. J Chem Neuroanat 42:242–248
37. Nopparat C, Porter JE, Ebadi M, Govitrapong P (2010) The mechanism for the neuroprotective effect of melatonin against methamphetamine-induced autophagy. J Pineal Res 49:382–389
38. Jeong JK, Moon MH, Lee YJ, Seol JW, Park SY (2012) Melatonin-induced autophagy protects against human prion protein-mediated neurotoxicity. J Pineal Res 53:138–146
39. Zheng Y, Hou J, Liu J, Yao M, Li L, Zhang B, Zhu H, Wang Z (2014) Inhibition of autophagy contributes to melatonin-mediated neuroprotection against transient focal cerebral ischemia in rats. J Pharmacol Sci 124:354–364
40. Zhou H, Chen J, Lu X, Shen C, Zeng J, Chen L, Pei Z (2012) Melatonin protects against rotenone-induced cell injury via inhibition of Omi and Bax-mediated autophagy in Hela cells. J Pineal Res 52:120–127
41. Clough RL, Dermentzaki G, Haritou M, Petsakou A, Stefanis L (2011) Regulation of α-synuclein expression in cultured cortical neurons. J Neurochem 117:275–285
42. Liu G, Wang P, Li X, Li Y, Xu S, Uéda K, Chan P, Yu S (2013) α-Synuclein promotes early neurite outgrowth in cultured primary neurons. J Neural Transm 120:1331–1343
43. Longo B, Vezzani A, Mello LE (2005) Growth-associated protein 43 expression in hippocampal molecular layer of chronic epileptic rats treated with cycloheximide. Epilepsia Suppl 5:125–128
44. Maekawa F, Tsuboi T, Oya M, Aung KH, Tsukahara S, Pellerin L, Nohara K (2013) Effects of sodium arsenite on neurite outgrowth and glutamate AMPA receptor expression in mouse cortical neurons. Neurotoxicology 37:197–206
45. Aung KH, Kurihara R, Nakashima S, Maekawa F, Nohara K, Kobayashi T, Tsukahara S (2013) Inhibition of neurite outgrowth and alteration of cytoskeletal gene expression by sodium arsenite. Neurotoxicology 34:226–235
46. Janda E, Isidoro C, Carresi C, Mollace V (2012) Defective autophagy in Parkinson’s disease: role of oxidative stress. Mol Neurobiol 46:639–661
47. Lee J, Giordano S, Zhang J (2012) Autophagy, mitochondria and oxidative stress: cross-talk and redox signaling. Biochem J 41:523–540
48. Scarpulla RC, Vega RB, Kelly DP (2012) Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 23:459–466
49. Wareski P, Vaarmann A, Choubey V, Safiulina D, Liiv J, Kuum M, Kaasik A (2009) PGC-1α and PGC-1β regulate mitochondrial density in neurons. J Biol Chem 284:21379–21385
50. Vaughan RA, Mermier CM, Bisoffi M, Trujillo KA, Conn CA (2014) Dietary stimulators of the PGC-1 superfamily and mitochondrial biosynthesis in skeletal muscle. A mini-review. J Physiol Biochem 70:271–284
51. Guo P, Pi H, Xu S, Zhang L, Li Y, Li M, Cao Z, Tian L et al (2014) Melatonin improves mitochondrial function by promoting MT1/SIRT1/PGC-1 alpha-dependent mitochondrial biogenesis in cadmium-induced hepatotoxicity in vitro. Toxicol Sci 142:182–195
52. Teodoro BG, Baraldi FG, Sampaio IH, Bomfim LH, Queiroz AL, Passos MA, Carneiro EM, Alberici LC et al (2014) Melatonin prevents mitochondrial dysfunction and insulin resistance in rat skeletal muscle. J Pineal Res 57:155–167