Roles of zinc and metallothionein-3 in oxidative stress-induced lysosomal dysfunction, cell death, and autophagy in neurons and astrocytes

Molecular Brain

Volumn 3, Issue 1, 2010, Pages

  Lee, Sook Jeong ^a   Koh, Jae Young ^a  

^a University of Ulsan   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; METALLOTHIONEIN III; ZINC; GROWTH INHIBITOR; NERVE PROTEIN;

ASTROCYTE; AUTOPHAGY; BRAIN INJURY; BRAIN ISCHEMIA; CELL CULTURE; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CYTOTOXICITY; HUMAN; LYSOSOME; LYSOSOME MEMBRANE; MEMBRANE PERMEABILITY; MOLECULAR MECHANICS; NERVE CELL; NERVE CELL NECROSIS; NERVE FIBER GROWTH; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; ANIMAL; CYTOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; ASTROCYTES; AUTOPHAGY; HUMANS; LYSOSOMES; NERVE TISSUE PROTEINS; NEURONS; OXIDATIVE STRESS; ZINC;

EID: 77958147359     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-3-30     Document Type: Review

References (139)

1. Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection. NB Nedelsky PK Todd JP Taylor, Biochim Biophys Acta 2008 1782 691 699 18930136
2. Lysosomes and autophagy in cell death control. G Kroemer M Jaattela, Nat Rev Cancer 2005 5 886 897 10.1038/nrc1738 16239905
3. Peroxisome turnover by micropexophagy: an autophagy-related process. JC Farre S Subramani, Trends Cell Biol 2004 14 515 523 10.1016/j.tcb.2004.07.014 15350980
4. Autophagy: basic principles and relevance to disease. M Kundu CB Thompson, Annu Rev Pathol 2008 3 427 455 10.1146/annurev.pathmechdis.2.010506. 091842 18039129
5. The role of lysosomal rupture in neuronal death. T Yamashima S Oikawa, Prog Neurobiol 2009 89 343 358 10.1016/j.pneurobio.2009.09.003 19772886
6. Autophagy fights disease through cellular self-digestion. N Mizushima B Levine AM Cuervo DJ Klionsky, Nature 2008 451 1069 1075 10.1038/nature06639 18305538
7. Neuronal autophagy: going the distance to the axon. Z Yue QJ Wang M Komatsu, Autophagy 2008 4 94 96 18000396
8. Lysosomal release of cathepsins causes ischemic damage in the rat hippocampal slice and depends on NMDA-mediated calcium influx, arachidonic acid metabolism, and free radical production. JA Windelborn P Lipton, J Neurochem 2008 106 56 69 10.1111/j.1471-4159.2008.05349.x 18363826
9. Autophagic neuron death. Y Uchiyama M Koike M Shibata M Sasaki, Methods Enzymol 2009 453 33 51 19216901
10. Cell biology: autophagy and cancer. B Levine, Nature 2007 446 745 747 10.1038/446745a 17429391
11. Autophagy in the pathogenesis of disease. B Levine G Kroemer, Cell 2008 132 27 42 10.1016/j.cell.2007.12.018 18191218
12. Autophagy and protein aggregation after brain ischemia. C Liu Y Gao J Barrett B Hu, J Neurochem 2010 115 68 78 10.1111/j.1471-4159.2010.06905.x 20633207
13. Autophagy induced by ischemic preconditioning is essential for cardioprotection. C Huang S Yitzhaki CN Perry W Liu Z Giricz RM Mentzer Jr RA Gottlieb, J Cardiovasc Transl Res 2010 3 365 373 10.1007/s12265-010-9189-3 20559777
14. Zinc(II) ion mediates tamoxifen-induced autophagy and cell death in MCF-7 breast cancer cell line. JJ Hwang HN Kim J Kim DH Cho MJ Kim YS Kim Y Kim SJ Park JY Koh, Biometals 20524045
15. Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. L Chakrabarti J Eng N Ivanov GA Garden AR La Spada, Mol Brain 2009 2 24 10.1186/1756-6606-2-24 19640278
16. Autophagy as a cell death and tumor suppressor mechanism. D Gozuacik A Kimchi, Oncogene 2004 23 2891 2906 10.1038/sj.onc.1207521 15077152
17. Autophagy in cancer and chemotherapy. S Yousefi HU Simon, Results Probl Cell Differ 2009 49 183 190 19142622
18. Reduced autophagic activity in primary rat hepatocellular carcinoma and ascites hepatoma cells. GO Kisen L Tessitore P Costelli PB Gordon PE Schwarze FM Baccino PO Seglen, Carcinogenesis 1993 14 2501 2505 10.1093/carcin/14.12.2501 8269618 (Pubitemid 24016585)
19. Bevacizumab and rapamycin inhibit tumor growth in peritoneal model of human ovarian cancer. H Huynh CC Teo KC Soo, Mol Cancer Ther 2007 6 2959 2966 10.1158/1535-7163.MCT-07-0237 18025280
20. Autophagy is activated by TGF-beta and potentiates TGF-beta-mediated growth inhibition in human hepatocellular carcinoma cells. K Kiyono HI Suzuki H Matsuyama Y Morishita A Komuro MR Kano K Sugimoto K Miyazono, Cancer Res 2009 69 8844 8852 10.1158/0008-5472.CAN-08-4401 19903843
21. Induction of autophagy and inhibition of tumorigenesis by beclin 1. XH Liang S Jackson M Seaman K Brown B Kempkes H Hibshoosh B Levine, Nature 1999 402 672 676 10.1038/45257 10604474
22. Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1 -/- mouse brain. G Liao Y Yao J Liu Z Yu S Cheung A Xie X Liang X Bi, Am J Pathol 2007 171 962 975 10.2353/ajpath.2007.070052 17631520
23. The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson's disease. T Pan S Kondo W Le J Jankovic, Brain 2008 131 1969 1978 10.1093/brain/awm318 18187492
24. Autophagy in neurodegeneration and development. AR Winslow DC Rubinsztein, Biochim Biophys Acta 2008 1782 723 729 18644437
25. The emerging role of autophagy in Parkinson's disease. ZH Cheung NY Ip, Mol Brain 2009 2 29 10.1186/1756-6606-2-29 19754977
26. Rapid and direct transport of cell surface APP to the lysosome defines a novel selective pathway. A Lorenzen J Samosh K Vandewark PH Anborgh C Seah AC Magalhaes SP Cregan SS Ferguson SH Pasternak, Mol Brain 2010 3 11 10.1186/1756-6606-3-11 20409323
27. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. T Hara K Nakamura M Matsui A Yamamoto Y Nakahara R Suzuki-Migishima M Yokoyama K Mishima I Saito H Okano,, et al. Nature 2006 441 885 889 10.1038/nature04724 16625204
28. Autophagy in neurodegeneration: two sides of the same coin. JA Lee, BMB Rep 2009 42 324 330 19558789
29. Zinc and 4-hydroxy-2-nonenal mediate lysosomal membrane permeabilization induced by H2O2 in cultured hippocampal neurons. JJ Hwang SJ Lee TY Kim JH Cho JY Koh, J Neurosci 2008 28 3114 3122 10.1523/JNEUROSCI.0199-08.2008 18354014
30. Oxidative injury triggers autophagy in astrocytes: the role of endogenous zinc. SJ Lee KS Cho JY Koh, Glia 2009 57 1351 1361 10.1002/glia.20854 19229997
31. Metallothionein-3 regulates lysosomal function in cultured astrocytes under both normal and oxidative conditions. SJ Lee MH Park HJ Kim JY Koh, Glia 2010 58 1186 1196 10.1002/glia.20905 20544854
32. The role of zinc in growth and cell proliferation. RS MacDonald, J Nutr 2000 130 1500S 1508S 10801966
33. Zinc in growth and development and spectrum of human zinc deficiency. AS Prasad, J Am Coll Nutr 1988 7 377 384 3053862
34. Zinc deficiency in the weanling rat: effects on liver composition and polysomal profiles. GJ Fosmire MA Fosmire HH Sanstead, J Nutr 1976 106 1152 1158 939995
35. The neurobiology of zinc in health and disease. CJ Frederickson JY Koh AI Bush, Nat Rev Neurosci 2005 6 449 462 10.1038/nrn1671 15891778
36. Human zinc deficiency, endocrine manifestations and response to treatment. HH Sandstead AS Prasad AR Schulert Z Farid A Miale Jr S Bassilly WJ Darby, Am J Clin Nutr 1967 20 422 442 6023853
37. The role of zinc in selective neuronal death after transient global cerebral ischemia. JY Koh SW Suh BJ Gwag YY He CY Hsu DW Choi, Science 1996 272 1013 1016 10.1126/science.272.5264.1013 8638123
38. Zinc and brain injury. DW Choi JY Koh, Annu Rev Neurosci 1998 21 347 375 10.1146/annurev.neuro.21.1.347 9530500
39. Zinc and excitotoxic brain injury: a new model. CJ Frederickson W Maret MP Cuajungco, Neuroscientist 2004 10 18 25 10.1177/1073858403255840 14987444
40. Zinc dyshomeostasis: a key modulator of neuronal injury. M Capasso JM Jeng M Malavolta E Mocchegiani SL Sensi, J Alzheimers Dis 2005 8 93 108 discussion 209-115 16308478
41. Zn2+ entry produces oxidative neuronal necrosis in cortical cell cultures. EY Kim JY Koh YH Kim S Sohn E Joe BJ Gwag, Eur J Neurosci 1999 11 327 334 10.1046/j.1460-9568.1999.00437.x 9987035
42. Zinc and disease of the brain. JY Koh, Mol Neurobiol 2001 24 99 106 10.1385/MN:24:1-3:099 11831557
43. Crosstalk between nitric oxide and zinc pathways to neuronal cell death involving mitochondrial dysfunction and p38-activated K+ channels. E Bossy-Wetzel MV Talantova WD Lee MN Scholzke A Harrop E Mathews T Gotz J Han MH Ellisman GA Perkins,, et al. Neuron 2004 41 351 365 10.1016/S0896-6273(04)00015- 7 14766175
44. ERK signaling leads to mitochondrial dysfunction in extracellular zinc-induced neurotoxicity. K He E Aizenman, J Neurochem 2010 114 452 461 20412391
45. Zn2+-induced ERK activation mediated by reactive oxygen species causes cell death in differentiated PC12 cells. SR Seo SA Chong SI Lee JY Sung YS Ahn KC Chung JT Seo, J Neurochem 2001 78 600 610 10.1046/j.1471-4159.2001.00438.x 11483663
46. The role of NADPH oxidase, neuronal nitric oxide synthase and poly(ADP ribose) polymerase in oxidative neuronal death induced in cortical cultures by brain-derived neurotrophic factor and neurotrophin-4/5. JJ Hwang SY Choi JY Koh, J Neurochem 2002 82 894 902 10.1046/j.1471-4159.2002.01040.x 12358795
47. Zinc inhibits astrocyte glutamate uptake by activation of poly(ADP-ribose) polymerase-1. SW Suh K Aoyama CC Alano CM Anderson AM Hamby RA Swanson, Mol Med 2007 13 344 349 10.2119/2007-00043.Suh 17728843
48. NADE, a p75NTR-associated cell death executor, is involved in signal transduction mediated by the common neurotrophin receptor p75NTR. J Mukai T Hachiya S Shoji-Hoshino MT Kimura D Nadano P Suvanto T Hanaoka Y Li S Irie LA Greene,, et al. J Biol Chem 2000 275 17566 17570 10.1074/jbc.C000140200 10764727
49. Co-induction of p75NTR and p75NTR-associated death executor in neurons after zinc exposure in cortical culture or transient ischemia in the rat. JA Park JY Lee TA Sato JY Koh, J Neurosci 2000 20 9096 9103 11124986
50. Zn(2+) induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. D Jiang PG Sullivan SL Sensi O Steward JH Weiss, J Biol Chem 2001 276 47524 47529 10.1074/jbc.M108834200 11595748
51. Cellular transporters for zinc. ED Harris, Nutr Rev 2002 60 121 124 10.1301/00296640260085877 12002684
52. Mammalian zinc transporters. JP Liuzzi RJ Cousins, Annu Rev Nutr 2004 24 151 172 10.1146/annurev.nutr.24.012003.132402 15189117
53. The function of zinc metallothionein: a link between cellular zinc and redox state. W Maret, J Nutr 2000 130 1455S 1458S 10801959
54. Growth-inhibitory factor, metallothionein-like protein, and neurodegenerative diseases. Y Uchida, Biol Signals 1994 3 211 215 10.1159/000109547 7834016
55. Cellular zinc and redox states converge in the metallothionein/thionein pair. W Maret, J Nutr 2003 133 1460S 1462S 12730443
56. Metallothionein in the central nervous system: Roles in protection, regeneration and cognition. AK West J Hidalgo D Eddins ED Levin M Aschner, Neurotoxicology 2008 29 489 503 10.1016/j.neuro.2007.12.006 18313142
57. The growth inhibitory factor that is deficient in the Alzheimer's disease brain is a 68 amino acid metallothionein-like protein. Y Uchida K Takio K Titani Y Ihara M Tomonaga, Neuron 1991 7 337 347 10.1016/0896-6273(91)90272-2 1873033
58. Cytoarchitectonic distribution of zinc in the hippocampus of man and the rat. CJ Frederickson MA Klitenick WI Manton JB Kirkpatrick, Brain Res 1983 273 335 339 10.1016/0006-8993(83)90858-2 6616240
59. Imaging free zinc in synaptic terminals in live hippocampal slices. T Budde A Minta JA White AR Kay, Neuroscience 1997 79 347 358 10.1016/S0306- 4522(96)00695-1 9200720
60. The dithizone, Timm's sulphide silver and the selenium methods demonstrate a chelatable pool of zinc in CNS. A proton activation (PIXE) analysis of carbon tetrachloride extracts from rat brains and spinal cords intravitally treated with dithizone. G Danscher G Howell J Perez-Clausell N Hertel, Histochemistry 1985 83 419 422 10.1007/BF00509203 3000994
61. Importance of zinc in the central nervous system: the zinc-containing neuron. CJ Frederickson SW Suh D Silva RB Thompson, J Nutr 2000 130 1471S 1483S 10801962
62. Release of endogenous Zn2+ from brain tissue during activity. SY Assaf SH Chung, Nature 1984 308 734 736 10.1038/308734a0 6717566
63. Synaptically released zinc: physiological functions and pathological effects. CJ Frederickson AI Bush, Biometals 2001 14 353 366 10.1023/A: 1012934207456 11831465
64. Stimulation-induced uptake and release of zinc in hippocampal slices. GA Howell MG Welch CJ Frederickson, Nature 1984 308 736 738 10.1038/308736a0 6717567
65. AMPA receptor activation potentiates zinc neurotoxicity. JH Weiss DM Hartley JY Koh DW Choi, Neuron 1993 10 43 49 10.1016/0896-6273(93)90240-R 7678965
66. Zinc toxicity on cultured cortical neurons: involvement of N-methyl-D-aspartate receptors. JY Koh DW Choi, Neuroscience 1994 60 1049 1057 10.1016/0306-4522(94)90282-8 7936205
67. Oligodendrocytes and ischemic brain injury. D Dewar SM Underhill MP Goldberg, J Cereb Blood Flow Metab 2003 23 263 274 10.1097/00004647-200303000- 00001 12621301
68. Essential cellular regulatory elements of oxidative stress in early and late phases of apoptosis in the central nervous system. ZZ Chong JQ Kang K Maiese, Antioxid Redox Signal 2004 6 277 287 10.1089/152308604322899341 15025929
69. Neuronal and glial apoptosis in human traumatic brain injury. J Dressler U Hanisch E Kuhlisch KD Geiger, Int J Legal Med 2007 121 365 375 10.1007/s00414-006-0126-6 17106737
70. Astrocyte metabolism and signaling during brain ischemia. DJ Rossi JD Brady C Mohr, Nat Neurosci 2007 10 1377 1386 10.1038/nn2004 17965658
71. Translocation of zinc may contribute to seizure-induced death of neurons. CJ Frederickson MD Hernandez JF McGinty, Brain Res 1989 480 317 321 10.1016/0006-8993(89)90199-6 2713657
72. Loss of zinc staining from hippocampal mossy fibers during kainic acid induced seizures: a histofluorescence study. CJ Frederickson MD Hernandez SA Goik JD Morton JF McGinty, Brain Res 1988 446 383 386 10.1016/0006-8993(88) 90899-2 3370496
73. Accumulation of zinc in degenerating hippocampal neurons of ZnT3-null mice after seizures: evidence against synaptic vesicle origin. JY Lee TB Cole RD Palmiter JY Koh, J Neurosci 2000 20 C79 10807937
74. Evidence that synaptically-released zinc contributes to neuronal injury after traumatic brain injury. SW Suh JW Chen M Motamedi B Bell K Listiak NF Pons G Danscher CJ Frederickson, Brain Res 2000 852 268 273 10.1016/S0006-8993(99) 02095-8 10678752
75. Possible role of zinc in the selective degeneration of dentate hilar neurons after cerebral ischemia in the adult rat. N Tonder FF Johansen CJ Frederickson J Zimmer NH Diemer, Neurosci Lett 1990 109 247 252 10.1016/0304-3940(90)90002-Q 2330128
76. Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. TB Cole HJ Wenzel KE Kafer PA Schwartzkroin RD Palmiter, Proc Natl Acad Sci USA 1999 96 1716 1721 10.1073/pnas.96.4.1716 9990090
77. Zinc released from metallothionein-iii may contribute to hippocampal CA1 and thalamic neuronal death following acute brain injury. JY Lee JH Kim RD Palmiter JY Koh, Exp Neurol 2003 184 337 347 10.1016/S0014-4886(03)00382-0 14637104
78. Cytosolic labile zinc: a marker for apoptosis in the developing rat brain. JY Lee JJ Hwang MH Park JY Koh, Eur J Neurosci 2006 23 435 442 10.1111/j.1460-9568.2005.04553.x 16420450
79. Intracellular Zn2+ accumulation contributes to synaptic failure, mitochondrial depolarization, and cell death in an acute slice oxygen-glucose deprivation model of ischemia. YV Medvedeva B Lin CW Shuttleworth JH Weiss, J Neurosci 2009 29 1105 1114 10.1523/JNEUROSCI.4604-08.2009 19176819
80. Glutamate neurotoxicity in cortical cell culture is calcium dependent. DW Choi, Neurosci Lett 1985 58 293 297 10.1016/0304-3940(85)90069-2 2413399
81. Calcium-dependent mitochondrial function and dysfunction in neurons. NB Pivovarova SB Andrews, FEBS J 20659161
82. Intracellular zinc elevation measured with a "calcium-specific" indicator during ischemia and reperfusion in rat hippocampus: a question on calcium overload. CJ Stork YV Li, J Neurosci 2006 26 10430 10437 10.1523/JNEUROSCI.1588-06.2006 17035527
83. AMPA/kainate receptors in mouse spinal cord cell-specific display of receptor subunits by oligodendrocytes and astrocytes and at the nodes of Ranvier. E Brand-Schieber P Werner, Glia 2003 42 12 24 10.1002/glia.10136 12594733
84. Glutamate exocytosis from astrocytes controls synaptic strength. P Jourdain LH Bergersen K Bhaukaurally P Bezzi M Santello M Domercq C Matute F Tonello V Gundersen A Volterra, Nat Neurosci 2007 10 331 339 10.1038/nn1849 17310248
85. Excitotoxic damage to white matter. C Matute E Alberdi M Domercq MV Sanchez-Gomez A Perez-Samartin A Rodriguez-Antiguedad F Perez-Cerda, J Anat 2007 210 693 702 10.1111/j.1469-7580.2007.00733.x 17504270
86. Pyruvate protects against kainate-induced epileptic brain damage in rats. TY Kim JS Yi SJ Chung DK Kim HR Byun JY Lee JY Koh, Exp Neurol 2007 208 159 167 10.1016/j.expneurol.2007.08.013 17905231
87. Elements of cerebral microvascular ischaemia. MA Petty JG Wettstein, Brain Res Brain Res Rev 2001 36 23 34 10.1016/S0165-0173(01)00062-5 11516770
88. Protection by pyruvate against transient forebrain ischemia in rats. JY Lee YH Kim JY Koh, J Neurosci 2001 21 C171 11588201
89. Zinc translocation accelerates infarction after mild transient focal ischemia. JM Lee GJ Zipfel KH Park YY He CY Hsu DW Choi, Neuroscience 2002 115 871 878 10.1016/S0306-4522(02)00513-4 12435425
90. Oxidative stress in brain ischemia. S Love, Brain Pathol 1999 9 119 131 10.1111/j.1750-3639.1999.tb00214.x 9989455
91. Zinc-induced neuronal death in cortical neurons. D Lobner LM Canzoniero P Manzerra F Gottron H Ying M Knudson M Tian LL Dugan GA Kerchner CT Sheline,, et al. Cell Mol Biol (Noisy-le-grand) 2000 46 797 806 10875441
92. Lysosomal membrane permeabilization in cell death. P Boya G Kroemer, Oncogene 2008 27 6434 6451 10.1038/onc.2008.310 18955971
93. Regulation of apoptosis-associated lysosomal membrane permeabilization. AC Johansson H Appelqvist C Nilsson K Kagedal K Roberg K Ollinger, Apoptosis 2010 15 527 540 10.1007/s10495-009-0452-5 20077016
94. Autophagy, bafilomycin and cell death: the "a-B-cs" of plecomacrolide-induced neuroprotection. JJ Shacka BJ Klocke KA Roth, Autophagy 2006 2 228 230 16874105
95. Bafilomycin A1 inhibits chloroquine-induced death of cerebellar granule neurons. JJ Shacka BJ Klocke M Shibata Y Uchiyama G Datta RE Schmidt KA Roth, Mol Pharmacol 2006 69 1125 1136 10.1124/mol.105.018408 16391239
96. Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis'. T Yamashima Y Kohda K Tsuchiya T Ueno J Yamashita T Yoshioka E Kominami, Eur J Neurosci 1998 10 1723 1733 10.1046/j.1460-9568.1998.00184.x 9751144
97. Peroxisome proliferator-activated receptor gamma-independent activation of p38 MAPK by thiazolidinediones involves calcium/calmodulin-dependent protein kinase II and protein kinase R: correlation with endoplasmic reticulum stress. OS Gardner CW Shiau CS Chen LM Graves, J Biol Chem 2005 280 10109 10118 10.1074/jbc.M410445200 15649892
98. Endoplasmic reticulum stress stimulates the expression of cyclooxygenase-2 through activation of NF-kappaB and pp38 mitogen-activated protein kinase. JH Hung IJ Su HY Lei HC Wang WC Lin WT Chang W Huang WC Chang YS Chang CC Chen,, et al. J Biol Chem 2004 279 46384 46392 10.1074/jbc.M403568200 15319438
99. Elevation of intracellular calcium ions is essential for the H2O2-induced activation of SAPK/JNK but not for that of p38 and ERK in Chinese hamster V79 cells. O Inanami T Ohta S Ito M Kuwabara, Antioxid Redox Signal 1999 1 501 508 10.1089/ars.1999.1.4-501 11233147
100. The cellular response to protein misfolding in the endoplasmic reticulum. AA Welihinda W Tirasophon RJ Kaufman, Gene Expr 1999 7 293 300 10440230
101. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. I Kim W Xu JC Reed, Nat Rev Drug Discov 2008 7 1013 1030 10.1038/nrd2755 19043451
102. Life, death and burial: multifaceted impact of autophagy. L Galluzzi E Morselli JM Vicencio O Kepp N Joza N Tajeddine G Kroemer, Biochem Soc Trans 2008 36 786 790 10.1042/BST0360786 18793137
103. Selective degradation of mitochondria by mitophagy. I Kim S Rodriguez-Enriquez JJ Lemasters, Arch Biochem Biophys 2007 462 245 253 10.1016/j.abb.2007.03.034 17475204
104. The molecular machinery of autophagy: unanswered questions. DJ Klionsky, J Cell Sci 2005 118 7 18 10.1242/jcs.01620 15615779
105. Autophagy: in sickness and in health. AM Cuervo, Trends Cell Biol 2004 14 70 77 10.1016/j.tcb.2003.12.002 15102438
106. The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. ET Bampton CG Goemans D Niranjan N Mizushima AM Tolkovsky, Autophagy 2005 1 23 36 10.4161/auto.1.1.1495 16874023
107. Effects of dopamine on LC3-II activation as a marker of autophagy in a neuroblastoma cell model. P Gimenez-Xavier R Francisco AF Santidrian J Gil S Ambrosio, Neurotoxicology 2009 30 658 665 10.1016/j.neuro.2009.04.007 19410601
108. The protein-binding potential of C2H2 zinc finger domains. KJ Brayer S Kulshreshtha DJ Segal, Cell Biochem Biophys 2008 51 9 19 10.1007/s12013-008- 9007-6 18286240
109. Mammalian zinc transport, trafficking, and signals. RJ Cousins JP Liuzzi LA Lichten, J Biol Chem 2006 281 24085 24089 10.1074/jbc.R600011200 16793761
110. The zinc/thiolate redox biochemistry of metallothionein and the control of zinc ion fluctuations in cell signaling. A Krezel Q Hao W Maret, Arch Biochem Biophys 2007 463 188 200 10.1016/j.abb.2007.02.017 17391643
111. Zinc coordination environments in proteins as redox sensors and signal transducers. W Maret, Antioxid Redox Signal 2006 8 1419 1441 10.1089/ars.2006.8.1419 16987000
112. Metallothionein redox biology in the cytoprotective and cytotoxic functions of zinc. W Maret, Exp Gerontol 2008 43 363 369 10.1016/j.exger.2007. 11.005 18171607
113. Cell death in the injured brain: roles of metallothioneins. MO Pedersen A Larsen M Stoltenberg M Penkowa, Prog Histochem Cytochem 2009 44 1 27 10.1016/j.proghi.2008.10.002 19348909
114. Metallothionein expression by NG2 glial cells following CNS injury. RS Chung SJ Fung YK Leung AK Walker GH McCormack MI Chuah JC Vickers AK West, Cell Mol Life Sci 2007 64 2716 2722 10.1007/s00018-007-7267-8 17896077
115. Interactions between metallothionein and trace elements. I Bremner, Prog Food Nutr Sci 1987 11 1 37 3303133
116. Oxygen free radicals and metallothionein. M Sato I Bremner, Free Radic Biol Med 1993 14 325 337 10.1016/0891-5849(93)90029-T 8458590
117. Metallothionein and a peptide modeled after metallothionein, EmtinB, induce neuronal differentiation and survival through binding to receptors of the low-density lipoprotein receptor family. M Ambjorn JW Asmussen M Lindstam K Gotfryd C Jacobsen VV Kiselyov SK Moestrup M Penkowa E Bock V Berezin, J Neurochem 2008 104 21 37 17986228
118. Intraneuronal signaling pathways of metallothionein. JW Asmussen ML Von Sperling M Penkowa, J Neurosci Res 2009 87 2926 2936 10.1002/jnr.22118 19405100
119. Signal transduction in monocytes: the role of zinc ions. H Haase L Rink, Biometals 2007 20 579 585 10.1007/s10534-006-9029-8 17453150
120. Metallothionein induces a regenerative reactive astrocyte phenotype via JAK/STAT and RhoA signalling pathways. YK Leung M Pankhurst SA Dunlop S Ray J Dittmann ED Eaton P Palumaa R Sillard MI Chuah AK West,, et al. Exp Neurol 2010 221 98 106 10.1016/j.expneurol.2009.10.006 19837066
121. The metallothionein/thionein system: an oxidoreductive metabolic zinc link. SG Bell BL Vallee, Chembiochem 2009 10 55 62 10.1002/cbic.200800511 19089881
122. Neuronal growth-inhibitory factor (metallothionein-3): structure-function relationships. ZC Ding FY Ni ZX Huang, FEBS J 2010 277 2912 2920 10.1111/j.1742-4658.2010.07716.x 20561055
123. Neuronal growth-inhibitory factor (metallothionein-3): reactivity and structure of metal-thiolate clusters. P Faller, FEBS J 2010 277 2921 2930 10.1111/j.1742-4658.2010.07717.x 20561054
124. Metallothioneins: historical review and state of knowledge. M Nordberg, Talanta 1998 46 243 254 10.1016/S0039-9140(97)00345-7 18967148
125. Metallothionein isoform 3 expression in the human prostate and cancer-derived cell lines. SH Garrett MA Sens D Shukla S Nestor S Somji JH Todd DA Sens, Prostate 1999 41 196 202 10.1002/(SICI)1097-0045(19991101)41:3<196:: AID-PROS7>3.0.CO;2-U 10517878
126. Expression of MT-3 protein in the human kidney. SH Garrett MA Sens JH Todd S Somji DA Sens, Toxicol Lett 1999 105 207 214 10.1016/S0378-4274(99)00003- X 10355541
127. Expression of MT-3 mRNA in human kidney, proximal tubule cell cultures, and renal cell carcinoma. JG Hoey SH Garrett MA Sens JH Todd DA Sens, Toxicol Lett 1997 92 149 160 10.1016/S0378-4274(97)00049-0 9295238
128. Expression of the gene encoding metallothionein-3 in organs of the reproductive system. P Moffatt C Seguin, DNA Cell Biol 1998 17 501 510 10.1089/dna.1998.17.501 9655243
129. Bioactivity of metallothionein-3 correlates with its novel beta domain sequence rather than metal binding properties. AK Sewell LT Jensen JC Erickson RD Palmiter DR Winge, Biochemistry 1995 34 4740 4747 10.1021/bi00014a031 7718580
130. Metallothionein-IIA promotes neurite growth via the megalin receptor. M Fitzgerald P Nairn CA Bartlett RS Chung AK West LD Beazley, Exp Brain Res 2007 183 171 180 10.1007/s00221-007-1032-y 17634932
131. Peptides modeled after the alpha-domain of metallothionein induce neurite outgrowth and promote survival of cerebellar granule neurons. JW Asmussen M Ambjorn E Bock V Berezin, Eur J Cell Biol 2009 88 433 443 10.1016/j.ejcb.2009. 04.001 19446362
132. Developmental immunohistochemistry of growth inhibitory factor in normal brains and brains of patients with Down syndrome. Y Arai Y Uchida S Takashima, Pediatr Neurol 1997 17 134 138 10.1016/S0887-8994(97)00085-4 9367293
133. Neuron death and glial response in pontosubicular necrosis. The role of the growth inhibition factor. H Isumi Y Uchida T Hayashi S Furukawa S Takashima, Clin Neuropathol 2000 19 77 84 10749288
134. Differential expression of metallothioneins in human prion diseases. T Kawashima K Doh-ura M Torisu Y Uchida A Furuta T Iwaki, Dement Geriatr Cogn Disord 2000 11 251 262 10.1159/000017247 10940676
135. Disruption of the metallothionein-III gene in mice: analysis of brain zinc, behavior, and neuron vulnerability to metals, aging, and seizures. JC Erickson G Hollopeter SA Thomas GJ Froelick RD Palmiter, J Neurosci 1997 17 1271 1281 9006971
136. Role of metallothionein-III following central nervous system damage. J Carrasco M Penkowa M Giralt J Camats A Molinero IL Campbell RD Palmiter J Hidalgo, Neurobiol Dis 2003 13 22 36 10.1016/S0969-9961(03)00015-9 12758064
137. Disease progression in a transgenic model of familial amyotrophic lateral sclerosis is dependent on both neuronal and non-neuronal zinc binding proteins. K Puttaparthi WL Gitomer U Krishnan M Son B Rajendran JL Elliott, J Neurosci 2002 22 8790 8796 12388585
138. Role of metallothioneins in peripheral nerve function and regeneration. D Ceballos N Lago E Verdu M Penkowa J Carrasco X Navarro RD Palmiter J Hidalgo, Cell Mol Life Sci 2003 60 1209 1216 12861386
139. Abl kinases regulate autophagy by promoting the trafficking and function of lysosomal components. G Yogalingam AM Pendergast, J Biol Chem 2008 283 35941 35953 10.1074/jbc.M804543200 18945674