Autophagy Plays a Cytoprotective Role During Cadmium-Induced Oxidative Damage in Primary Neuronal Cultures

Biological Trace Element Research

Volumn 168, Issue 2, 2015, Pages 481-489

  Wang, Tao ^a   Wang, Qiwen ^a,b   Song, Ruilong ^a   Zhang, Yajing ^a   Zhang, Kangbao ^a   Yuan, Yan ^a   Bian, Jianchun ^a   Liu, Xuezhong ^a   Gu, Jianhong ^a   Liu, Zongping ^a  

^a YANGZHOU UNIVERSITY   (China)

^b GUIZHOU UNIVERSITY OF ENGINEERING SCIENCE   (China)

Author keywords

Autophagy; Cadmium; Cortical neurons; Oxidative damage; Reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; CADMIUM; CHLOROQUINE; CYTOPLASM PROTEIN; LACTATE DEHYDROGENASE; PROTEIN LC3; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ANTIOXIDANT; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL COUNT; CELL ORGANELLE; CELL PROTECTION; FETUS; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL CULTURE; NERVE CELL LESION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; ANIMAL; BRAIN CORTEX; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; FLUORESCENCE MICROSCOPY; METABOLISM; NERVE CELL; PRIMARY CELL CULTURE; SPRAGUE DAWLEY RAT;

ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; AUTOPHAGY; CADMIUM; CELLS, CULTURED; CEREBRAL CORTEX; CHLOROQUINE; L-LACTATE DEHYDROGENASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; OXIDATIVE STRESS; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 84947032126     PISSN: 01634984     EISSN: 15590720     Source Type: Journal    
DOI: 10.1007/s12011-015-0390-8     Document Type: Article

References (42)

1. Chen H, Firestein BL (2007) RhoA regulates dendrite branching in hippocampal neurons by decreasing cypin protein levels. J Neurosci Off J Soc Neurosci 27(31):8378–8386. doi:10.1523/JNEUROSCI.0872-07.2007
2. Nakayama T, Mizoguchi T, Uehara S, Yamashita T, Kawahara I, Kobayashi Y, Moriyama Y, Kurihara S, Sahara N, Ozawa H, Udagawa N, Takahashi N (2011) Polarized osteoclasts put marks of tartrate-resistant acid phosphatase on dentin slices—a simple method for identifying polarized osteoclasts. Bone 49(6):1331–1339. doi:10.1016/j.bone.2011.09.045
3. Qin H, Liu T, Yang JL, Huang X, Liu B, Song X, Zhao X, Wei YQ (2007) Screening proteins related to retinoic acid resistance by proteomic analysis. Zhonghua Yi Xue Za Zhi 87(8):520–525
4. Patenaude A, Deschesnes RG, Rousseau JL, Petitclerc E, Lacroix J, Cote MF, CG R (2007) New soft alkylating agents with enhanced cytotoxicity against cancer cells resistant to chemotherapeutics and hypoxia. Cancer Res 67(5):2306–2316. doi:10.1158/0008-5472.CAN-06-3824
5. Huang CH, Cheng JC, Chen JC, Tseng CP (2007) Evaluation of the role of Disabled-2 in nerve growth factor-mediated neurite outgrowth and cellular signalling. Cell Signal 19(6):1339–1347. doi:10.1016/j.cellsig.2007.01.019
6. Prabu SM, Shagirtha K, Renugadevi J (2011) Naringenin in combination with vitamins C and E potentially protects oxidative stress-mediated hepatic injury in cadmium-intoxicated rats. J Nutr Sci Vitaminol 57(2):177–185
7. Haas MA, Vickers JC, Dickson TC (2007) Rho kinase activates ezrin-radixin-moesin (ERM) proteins and mediates their function in cortical neuron growth, morphology and motility in vitro. J Neurosci Res 85(1):34–46. doi:10.1002/jnr.21102
8. Lukawski K, Nieradko B, Sieklucka-Dziuba M (2005) Effects of cadmium on memory processes in mice exposed to transient cerebral oligemia. Neurotoxicol Teratol 27(4):575–584. doi:10.1016/j.ntt.2005.05.009
9. Nishimura Y, Yamaguchi JY, Kanada A, Horimoto K, Kanemaru K, Satoh M, Oyama Y (2006) Increase in intracellular Cd(2+) concentration of rat cerebellar granule neurons incubated with cadmium chloride: cadmium cytotoxicity under external Ca(2+)-free condition. Toxicol In Vitro Int J Publ Assoc BIBRA 20(2):211–216. doi:10.1016/j.tiv.2005.06.006
10. Paul BZ, Kim S, Dangelmaier C, Nagaswami C, Jin J, Hartwig JH, Weisel JW, Daniel JL, Kunapuli SP (2003) Dynamic regulation of microtubule coils in ADP-induced platelet shape change by p160ROCK (Rho-kinase). Platelets 14(3):159–169
11. Okuda B, Iwamoto Y, Tachibana H, Sugita M (1997) Parkinsonism after acute cadmium poisoning. Clin Neurol Neurosurg 99(4):263–265
12. Azad MB, Chen Y, Gibson SB (2009) Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 11(4):777–790. doi:10.1089/ARS.2008.2270
13. Scherz-Shouval R, Elazar Z (2011) Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 36(1):30–38. doi:10.1016/j.tibs.2010.07.007
14. Hu Y, Cui Q, Harvey AR (2007) Interactive effects of C3, cyclic AMP and ciliary neurotrophic factor on adult retinal ganglion cell survival and axonal regeneration. Mol Cell Neurosci 34(1):88–98. doi:10.1016/j.mcn.2006.10.005
15. Lee J, Giordano S, Zhang J (2012) Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441(2):523–540. doi:10.1042/BJ20111451
16. Luo YH, Wu SB, Wei YH, Chen YC, Tsai MH, Ho CC, Lin SY, Yang CS, Lin P (2013) Cadmium-based quantum dot induced autophagy formation for cell survival via oxidative stress. Chem Res Toxicol 26(5):662–673. doi:10.1021/tx300455k
17. Fukushima N, Morita Y (2006) Actomyosin-dependent microtubule rearrangement in lysophosphatidic acid-induced neurite remodeling of young cortical neurons. Brain Res 1094(1):65–75. doi:10.1016/j.brainres.2006.04.007
18. Shimoyama T, Hamano T, Natsume T, Koizumi F, Kiura K, Tanimoto M, Nishio K (2006) Reference profiling of the genomic response induced by an antimicrotubule agent, TZT-1027 (Soblidotin), in vitro. Pharmacogenomics J 6(6):388–396. doi:10.1038/sj.tpj.6500386
19. Ipe BI, Lehnig M, Niemeyer CM (2005) On the generation of free radical species from quantum dots. Small 1(7):706–709. doi:10.1002/smll.200500105
20. Gorovoy M, Niu J, Bernard O, Profirovic J, Minshall R, Neamu R, Voyno-Yasenetskaya T (2005) LIM kinase 1 coordinates microtubule stability and actin polymerization in human endothelial cells. J Biol Chem 280(28):26533–26542. doi:10.1074/jbc.M502921200
21. Rego AC, Oliveira CR (2003) Mitochondrial dysfunction and reactive oxygen species in excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases. Neurochem Res 28(10):1563–1574
22. Floyd RA (1999) Neuroinflammatory processes are important in neurodegenerative diseases: an hypothesis to explain the increased formation of reactive oxygen and nitrogen species as major factors involved in neurodegenerative disease development. Free Radic Biol Med 26(9–10):1346–1355
23. Wei X, Qi Y, Zhang X, Gu X, Cai H, Yang J, Zhang Y (2015) ROS act as an upstream signal to mediate cadmium-induced mitophagy in mouse brain. Neurotoxicology 46:19–24. doi:10.1016/j.neuro.2014.11.007
24. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26(7):1749–1760. doi:10.1038/sj.emboj.7601623
25. Okai T, Araki Y, Tada M, Tateno T, Kontani K, Katada T (2004) Novel small GTPase subfamily capable of associating with tubulin is required for chromosome segregation. J Cell Sci 117(Pt 20):4705–4715. doi:10.1242/jcs.01347
26. Boutillier S, Rapp J, Staeb T, Olenik C, Schmidt G, Meyer DK, Leemhuis J (2003) Cytotoxic necrotizing factor-2 of Escherichia coli alters the morphology of cultured hippocampal neurons. Naunyn Schmiedeberg’s Arch Pharmacol 368(6):513–519. doi:10.1007/s00210-003-0830-4
27. Buttner B, Kannicht C, Reutter W, Horstkorte R (2003) The neural cell adhesion molecule is associated with major components of the cytoskeleton. Biochem Biophys Res Commun 310(3):967–971
28. Nambu H, Nambu R, Melia M, Campochiaro PA (2003) Combretastatin A-4 phosphate suppresses development and induces regression of choroidal neovascularization. Invest Ophthalmol Vis Sci 44(8):3650–3655
29. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282(33):24131–24145. doi:10.1074/jbc.M702824200
30. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, Shimizu S (2009) Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461(7264):654–658. doi:10.1038/nature08455
31. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441(7095):880–884. doi:10.1038/nature04723
32. Sun K, Xie X, Liu Y, Han Z, Zhao X, Cai N, Zhang S, Song J, Wei L (2013) Autophagy lessens ischemic liver injury by reducing oxidative damage. Cell Biosci 3(1):26. doi:10.1186/2045-3701-3-26
33. Yuan Y, Jiang CY, Xu H, Sun Y, Hu FF, Bian JC, Liu XZ, Gu JH, Liu ZP (2013) Cadmium-induced apoptosis in primary rat cerebral cortical neurons culture is mediated by a calcium signaling pathway. PLoS One 8(5), e64330. doi:10.1371/journal.pone.0064330
34. Sakamoto M, Kondo A, Kawasaki K, Goto T, Sakamoto H, Miyake K, Koyamatsu Y, Akiya T, Iwabuchi H, Muroya T, Ochiai K, Tanaka T, Kikuchi Y, Tenjin Y (2001) Analysis of gene expression profiles associated with cisplatin resistance in human ovarian cancer cell lines and tissues using cDNA microarray. Hum Cell Off J Hum Cell Res Soc 14(4):305–315
35. Di Gioacchino M, Petrarca C, Perrone A, Farina M, Sabbioni E, Hartung T, Martino S, Esposito DL, Lotti LV, Mariani-Costantini R (2008) Autophagy as an ultrastructural marker of heavy metal toxicity in human cord blood hematopoietic stem cells. Sci Total Environ 392(1):50–58. doi:10.1016/j.scitotenv.2007.11.009
36. Del Pino J, Zeballos G, Anadon MJ, Capo MA, Diaz MJ, Garcia J, Frejo MT (2014) Higher sensitivity to cadmium induced cell death of basal forebrain cholinergic neurons: a cholinesterase dependent mechanism. Toxicology 325:151–159. doi:10.1016/j.tox.2014.09.004
37. Wang B, Du Y (2013) Cadmium and its neurotoxic effects. Oxidative Med Cell Longev 2013:898034. doi:10.1155/2013/898034
38. Chen L, Xu B, Liu L, Luo Y, Zhou H, Chen W, Shen T, Han X, Kontos CD, Huang S (2011) Cadmium induction of reactive oxygen species activates the mTOR pathway, leading to neuronal cell death. Free Radic Biol Med 50(5):624–632. doi:10.1016/j.freeradbiomed.2010.12.032
39. Yu Y, Duan J, Yu Y, Li Y, Liu X, Zhou X, Ho KF, Tian L, Sun Z (2014) Silica nanoparticles induce autophagy and autophagic cell death in HepG2 cells triggered by reactive oxygen species. J Hazard Mater 270:176–186. doi:10.1016/j.jhazmat.2014.01.028
40. Zhao Z, Han F, Yang S, Wu J, Zhan W (2015) Oxamate-mediated inhibition of lactate dehydrogenase induces protective autophagy in gastric cancer cells: involvement of the Akt-mTOR signaling pathway. Cancer Lett 358(1):17–26. doi:10.1016/j.canlet.2014.11.046
41. Kroemer G, Jaattela M (2005) Lysosomes and autophagy in cell death control. Nat Rev Cancer 5(11):886–897. doi:10.1038/nrc1738
42. Wang Q, Zhu J, Zhang K, Jiang C, Wang Y, Yuan Y, Bian J, Liu X, Gu J, Liu Z (2013) Induction of cytoprotective autophagy in PC-12 cells by cadmium. Biochem Biophys Res Commun 438(1):186–192. doi:10.1016/j.bbrc.2013.07.050