Cadmium-Induced Apoptosis in Primary Rat Cerebral Cortical Neurons Culture Is Mediated by a Calcium Signaling Pathway

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Yuan, Yan ^a   Jiang, Chen yang ^a   Xu, Hui ^a   Sun, Ya ^a   Hu, Fei fei ^a   Bian, Jian chun ^a   Liu, Xue zhong ^a   Gu, Jian hong ^a   Liu, Zong ping ^a  

^a YANGZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINOETHOXYDIPHENYLBORANE; ADENOSINE TRIPHOSPHATASE (CALCIUM MAGNESIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CADMIUM; CALCIUM CHELATING AGENT; CALCIUM ION; CASPASE 3; CASPASE 9; CASPASE INHIBITOR; CYTOCHROME C OXIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME SUBUNIT; HOMEOSTASIS; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT; UPREGULATION; WESTERN BLOTTING;

ACETATES; AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; BORON COMPOUNDS; CA(2+) MG(2+)-ATPASE; CADMIUM; CALCIUM; CALCIUM SIGNALING; CASPASE 3; CASPASE 9; CEREBRAL CORTEX; EGTAZIC ACID; ELECTRON TRANSPORT COMPLEX IV; FETUS; GENE EXPRESSION REGULATION; NEURONS; POLY(ADP-RIBOSE) POLYMERASES; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SODIUM-POTASSIUM-EXCHANGING ATPASE;

MURINAE; RATTUS;

EID: 84878552275     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064330     Document Type: Article

References (74)

1. Wu X, Liang Y, Jin T, Ye T, Kong Q, et al. (2008) Renal effects evolution in a Chinese population after reduction of cadmium exposure in rice. Environ Res 108: 233-238.
2. Oliveira H, Lopes T, Almeida T, Pereira Mde L, Santos C, (2012) Cadmium-induced genetic instability in mice testis. Hum Exp Toxicol 31: 1228-1236.
3. Baker JR, Edwards RJ, Lasker JM, Moore MR, Satarug S, (2005) Renal and hepatic accumulation of cadmium and lead in the expression of CYP4F2 and CYP2E1. Toxicol Lett 159: 182-191.
4. Lopez E, Arce C, Oset-Gasque MJ, Canadas S, Gonzalez MP, (2006) Cadmium induces reactive oxygenspecies generation and lipid peroxidation in cortical neurons in culture. Free Radic Biol Med 40: 940-951.
5. Coccini T, Barni S, Vaccarone R, Mustarelli P, Manzo L, et al. (2013) Pulmonary toxicity of instilled cadmium-doped silica nanoparticles during acute and subacute stages in rats. Histol Histopathol 28: 195-209.
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 (Tokyo) 57: 177-185.
7. Napolitano JR, Liu MJ, Bao S, Crawford M, Nana-Sinkam P, et al. (2012) Cadmium-mediated toxicity of lung epithelia is enhanced through NF-kappaB-mediated transcriptional activation of the human zinc transporter ZIP8. Am J Physiol Lung Cell Mol Physiol 302: L909-918.
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: 575-584.
9. Nishimura Y, Yamaguchi JY, Kanada A, Horimoto K, Kanemaru K, et al. (2006) Increase in intracellular Cd2+ concentration of rat cerebellar granule neurons incubated with cadmium chloride: cadmium cytotoxicity under external Ca2+-free condition. Toxicol In Vitro 20: 211-216.
10. Okuda B, Iwamoto Y, Tachibana H, Sugita M, (1997) Parkinsonism after acute cadmium poisoning. Clin Neurol Neurosurg 99: 263-265.
11. Jiang LF, Yao TM, Zhu ZL, Wang C, Ji LN, (2007) Impacts of Cd(II) on the conformation and self-aggregation of Alzheimer's tau fragment corresponding to the third repeat of microtubule-binding domain. Biochim Biophys Acta 1774: 1414-1421.
12. Son YO, Lee JC, Hitron JA, Pan J, Zhang Z, et al. (2010) Cadmium induces intracellular Ca2+- and H2O2-dependent apoptosis through JNK- and p53-mediated pathways in skin epidermal cell line. Toxicol Sci 113: 127-137.
13. Wang SH, Shih YL, Ko WC, Wei YH, Shih CM, (2008) Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell Mol Life Sci 65: 3640-3652.
14. Yeh JH, Huang CC, Yeh MY, Wang JS, Lee JK, et al. (2009) Cadmium-induced cytosolic Ca2+ elevation and subsequent apoptosis in renal tubular cells. Basic Clin Pharmacol Toxicol 104: 345-351.
15. Biagioli M, Pifferi S, Ragghianti M, Bucci S, Rizzuto R, et al. (2008) Endoplasmic reticulum stress and alteration in calcium homeostasis are involved in cadmium-induced apoptosis. Cell Calcium 43: 184-195.
16. Wang L, Cao J, Chen D, Liu X, Lu H, et al. (2009) Role of oxidative stress, apoptosis, and intracellular homeostasis in primary cultures of rat proximal tubular cells exposed to cadmium. Biol Trace Elem Res 127: 53-68.
17. Xu B, Chen S, Luo Y, Chen Z, Liu L, et al. (2011) Calcium signaling is involved in cadmium-induced neuronal apoptosis via induction of reactive oxygen species and activation of MAPK/mTOR network. PLoS One 6: e19052.
18. Berridge MJ, Bootman MD, Roderick HL, (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529.
19. Clapham DE, (2007) Calcium signaling. Cell 131: 1047-1058.
20. Thevenod F, Jones SW, (1992) Cadmium block of calcium current in frog sympathetic neurons. Biophys J 63: 162-168.
21. Beyersmann D, Hechtenberg S, (1997) Cadmium, gene regulation, and cellular signalling in mammalian cells. Toxicol Appl Pharmacol 144: 247-261.
22. Visser GJ, Peters PH, Theuvenet AP, (1993) Cadmium ion is a non-competitive inhibitor of red cell Ca2+-ATPase activity. Biochim Biophys Acta 1152: 26-34.
23. Wang SH, Shih YL, Lee CC, Chen WL, Lin CJ, et al. (2009) The role of endoplasmic reticulum in cadmium-induced mesangial cell apoptosis. Chem Biol Interact 181: 45-51.
24. Lohmann RD, Beyersmann D, (1993) Cadmium and zinc mediated changes of the Ca2+-dependent endonuclease in apoptosis. Biochem Biophys Res Commun 190: 1097-1103.
25. Misra UK, Gawdi G, Akabani G, Pizzo SV, (2002) Cadmium-induced DNA synthesis and cell proliferation in macrophages: the role of intracellular calcium and signal transduction mechanisms. Cell Signal 14: 327-340.
26. Long GJ, (1997) Cadmium perturbs calcium homeostasis in rat osteosarcoma (ROS 17/2.8) cells; a possible role for protein kinase C. Toxicol Lett. 91: 91-97.
27. Chacon E, Acosta D, (1991) Mitochondrial regulation of superoxide by Ca2+: an alternate mechanism for the cardiotoxicity of doxorubicin. Toxicol Appl Pharmacol 107: 117-128.
28. Ermak G, Davies KJ, (2002) Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol 38: 713-721.
29. Hossain S, Liu HN, Nguyen M, Shore G, Almazan G, (2009) Cadmium exposure induces mitochondria-dependent apoptosis in oligodendrocytes. Neurotoxicology 30: 544-554.
30. Krumschnabel G, Ebner HL, Hess MW, Villunger A, (2010) Apoptosis and necroptosis are induced in rainbow trout cell lines exposed to cadmium. Aquat Toxicol 99: 73-85.
31. Ferri KF, Kroemer G, (2001) Organelle-specific initiation of cell death pathways. Nat Cell Biol 3: E255-263.
32. Chatterjee S, Kundu S, Sengupta S, Bhattacharyya A, (2009) Divergence to apoptosis from ROS induced cell cycle arrest: effect of cadmium. Mutat Res 663: 22-31.
33. Cui ZG, Ogawa R, Piao JL, Hamazaki K, Feril LB Jr, et al. (2011) Molecular mechanisms involved in the adaptive response to cadmium-induced apoptosis in human myelomonocytic lymphoma U937 cells. Toxicol In Vitro 25: 1687-1693.
34. Yan Y, Bian JC, Zhong LX, Zhang Y, Sun Y, et al. (2012) Oxidative stress and apoptotic changes of rat cerebral cortical neurons exposed to cadmium in vitro. Biomed Environ Sci 25: 172-181.
35. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
36. Chen L, Liu L, Huang S, (2008) Cadmium activates the mitogen-activated protein kinase (MAPK) pathway via induction of reactive oxygen species and inhibition of protein phosphatases 2A and 5. Free Radic Biol Med 45: 1035-1044.
37. Chen L, Xu B, Liu L, Luo Y, Zhou H, et al. (2011) Cadmium induction of reactive oxygen species activates the mTOR pathway, leading to neuronal cell death. Free Radic Biol Med 50: 624-632.
38. Sohal RS, Toroser D, Bregere C, Mockett RJ, Orr WC, (2008) Age-related decrease in expression of mitochondrial DNA encoded subunits of cytochrome c oxidase in Drosophila melanogaster. Mech Ageing Dev 129: 558-561.
39. Garceau N, Pichaud N, Couture P, (2010) Inhibition of goldfish mitochondrial metabolism by in vitro exposure to Cd, Cu and Ni. Aquat Toxicol 98: 107-112.
40. Navarro A, Faria M, Barata C, Pina B, (2011) Transcriptional response of stress genes to metal exposure in zebra mussel larvae and adults. Environ Pollut 159: 100-107.
41. Wang L, Li J, Li J, Liu Z, (2010) Effects of lead and/or cadmium on the oxidative damage of rat kidney cortex mitochondria. Biol Trace Elem Res 137: 69-78.
42. Chen S, Xu Y, Xu B, Guo M, Zhang Z, et al. (2011) CaMKII is involved in cadmium activation of MAPK and mTOR pathways leading to neuronal cell death. J Neurochem 119: 1108-1118.
43. Neher E, Sakaba T, (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872.
44. Cheng A, Wang S, Yang D, Xiao R, Mattson MP, (2003) Calmodulin mediates brain-derived neurotrophic factor cell survival signaling upstream of Akt kinase in embryonic neocortical neurons. J Biol Chem 278: 7591-7599.
45. Surmeier DJ, Guzman JN, Sanchez-Padilla J, (2010) Calcium, cellular aging, and selective neuronal vulnerability in Parkinson's disease. Cell Calcium 47: 175-182.
46. Kawahara M, Kuroda Y, (2000) Molecular mechanism of neurodegeneration induced by Alzheimer's beta-amyloid protein: channel formation and disruption of calcium homeostasis. Brain Res Bull 53: 389-397.
47. Mattson MP, (2007) Calcium and neurodegeneration. Aging Cell 6: 337-350.
48. Marambaud P, Dreses-Werringloer U, Vingtdeux V, (2009) Calcium signaling in neurodegeneration. Mol Neurodegener 4: 20.
49. Fujita T, Inoue H, Kitamura T, Sato N, Shimosawa T, et al. (1998) Senescence marker protein-30 (SMP30) rescues cell death by enhancing plasma membrane Ca2+-pumping activity in Hep G2 cells. Biochem Biophys Res Commun 250: 374-380.
50. Sabolic I, (2006) Common mechanisms in nephropathy induced by toxic metals. Nephron Physiol 104: p107-114.
51. Xie Z, Zhang Y, Li A, Li P, Ji W, et al. (2010) Cd-induced apoptosis was mediated by the release of Ca2+ from intracellular Ca storage. Toxicol Lett 192: 115-118.
52. Ruiz A, Matute C, Alberdi E, (2009) Endoplasmic reticulum Ca2+ release through ryanodine and IP3 receptors contributes to neuronal excitotoxicity. Cell Calcium 46: 273-281.
53. Misra UK, Gawdi G, Pizzo SV, (2003) Induction of mitogenic signalling in the 1LN prostate cell line on exposure to submicromolar concentrations of cadmium+. Cell Signal 15: 1059-1070.
54. Deniaud A, Sharaf el dein O, Maillier E, Poncet D, Kroemer G, et al. (2008) Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene 27: 285-299.
55. Fleury C, Mignotte B, Vayssiere JL, (2002) Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84: 131-141.
56. Wallace DC, (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39: 359-407.
57. Onyango IG, Bennett JP Jr, Tuttle JB, (2005) Endogenous oxidative stress in sporadic Alzheimer's disease neuronal cybrids reduces viability by increasing apoptosis through pro-death signaling pathways and is mimicked by oxidant exposure of control cybrids. Neurobiol Dis 19: 312-322.
58. Foster KA, Galeffi F, Gerich FJ, Turner DA, Muller M, (2006) Optical and pharmacological tools to investigate the role of mitochondria during oxidative stress and neurodegeneration. Prog Neurobiol 79: 136-171.
59. Thevenod F, (2009) Cadmium and cellular signaling cascades: to be or not to be? Toxicol Appl Pharmacol 238: 221-239.
60. Fantin VR, Leder P, (2006) Mitochondriotoxic compounds for cancer therapy. Oncogene 25: 4787-4797.
61. Chakraborti T, Das S, Mondal M, Roychoudhury S, Chakraborti S, (1999) Oxidant, mitochondria and calcium: an overview. Cell Signal 11: 77-85.
62. Grammatopoulos TN, Johnson V, Moore SA, Andres R, Weyhenmeyer JA, (2004) Angiotensin type 2 receptor neuroprotection against chemical hypoxia is dependent on the delayed rectifier K+ channel, Na+/Ca2+ exchanger and Na+/K+ ATPase in primary cortical cultures. Neurosci Res 50: 299-306.
63. Kroemer G, Galluzzi L, Brenner C, (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163.
64. Tsujimoto Y, Shimizu S, (2000) Bcl-2 family: life-or-death switch. FEBS Lett 466: 6-10.
65. Matsumoto A, Isomoto H, Nakayama M, Hisatsune J, Nishi Y, et al. (2011) Helicobacter pylori VacA reduces the cellular expression of STAT3 and pro-survival Bcl-2 family proteins, Bcl-2 and Bcl-XL, leading to apoptosis in gastric epithelial cells. Dig Dis Sci 56: 999-1006.
66. Mertens HJ, Heineman MJ, Evers JL, (2002) The expression of apoptosis-related proteins Bcl-2 and Ki67 in endometrium of ovulatory menstrual cycles. Gynecol Obstet Invest 53: 224-230.
67. Cory S, Huang DC, Adams JM, (2003) The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22: 8590-8607.
68. Zhang H, Cai C, Shi C, Cao H, Han Z, et al. (2012) Cadmium-induced oxidative stress and apoptosis in the testes of frog Rana limnocharis. Aquat Toxicol 122-123: 67-74.
69. Lam M, Dubyak G, Chen L, Nunez G, Miesfeld RL, et al. (1994) Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc Natl Acad Sci U S A 91: 6569-6573.
70. Foyouzi-Youssefi R, Arnaudeau S, Borner C, Kelley WL, Tschopp J, et al. (2000) Bcl-2 decreases the free Ca2+ concentration within the endoplasmic reticulum. Proc Natl Acad Sci U S A 97: 5723-5728.
71. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X, (1999) Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15: 269-290.
72. Porter AG, Janicke RU, (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6: 99-104.
73. Kim J, Sharma RP, (2004) Calcium-mediated activation of c-Jun NH2-terminal kinase (JNK) and apoptosis in response to cadmium in murine macrophages. Toxicol Sci 81: 518-527.
74. Lopez E, Figueroa S, Oset-Gasque MJ, Gonzalez MP, (2003) Apoptosis and necrosis: two distinct events induced by cadmium in cortical neurons in culture. Br J Pharmacol 138: 901-911.