Cadmium induction of reactive oxygen species activates the mTOR pathway, leading to neuronal cell death

Free Radical Biology and Medicine

Volumn 50, Issue 5, 2011, Pages 624-632

  Chen, Long ^a,b   Xu, Baoshan ^a   Liu, Lei ^a   Luo, Yan ^a   Zhou, Hongyu ^a   Chen, Wenxing ^a   Shen, Tao ^a   Han, Xiuzhen ^a   Kontos, Christopher D ^c   Huang, Shile ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b NANJING NORMAL UNIVERSITY   (China)

^c DUKE UNIVERSITY   (United States)

Author keywords

AMP activated kinase; Apoptosis; Cadmium; Free radicals; Mammalian target of rapamycin; Phosphatase and tensin homologue deleted on chromosome 10; Reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; AMINOIMIDAZOLE CARBOXAMIDE RIBONUCLEOTIDE; CADMIUM CHLORIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN P22; PROTEIN P40; PROTEIN P47; PROTEIN P67; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; S6 KINASE; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ACETYLCYSTEINE; ANDROSTADIENES; ANIMALS; APOPTOSIS; CADMIUM; CARRIER PROTEINS; ENVIRONMENTAL POLLUTANTS; GENE EXPRESSION REGULATION; HUMANS; NADPH OXIDASE; NEURODEGENERATIVE DISEASES; NEURONS; PC12 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEINS; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; RATS; REACTIVE OXYGEN SPECIES; RECEPTORS, SOMATOMEDIN; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; TOR SERINE-THREONINE KINASES;

EUKARYOTA; MAMMALIA;

EID: 79551488995     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.12.032     Document Type: Article

References (50)

1. E. Lopez, C. Arce, M.J. Oset-Gasque, S. Canadas, and M.P. Gonzalez Cadmium induces reactive oxygen species generation and lipid peroxidation in cortical neurons in culture Free Radic. Biol. Med. 40 2006 940 951
2. M. Marlowe, A. Cossairt, C. Moon, J. Errera, A. MacNeel, R. Peak, J. Ray, and C. Schroeder Main and interaction effects of metallic toxins on classroom behavior J. Abnorm. Child Psychol. 13 1985 185 198
3. R. Pihl, and M. Parkes Hair element content in learning disabled children Science 198 1977 204 206
4. S. Kim, C. Moon, S. Eun, P. Ryu, and S. Jo Identification of ASK1, MKK4, JNK, c-Jun, and caspase-3 as a signaling cascade involved in cadmium-induced neuronal cell apoptosis Biochem. Biophys. Res. Commun. 328 2005 326 334
5. L.C. Baxter, D.L. Sparks, S.C. Johnson, B. Lenoski, J.E. Lopez, D.J. Connor, and M.N. Sabbagh Relationship of cognitive measures and gray and white matter in Alzheimers disease J. Alzheimers Dis. 9 2006 253 260
6. S. Johnson Gradual micronutrient accumulation and depletion in Alzheimers disease Med. Hypotheses 56 2001 595 597
7. Z. Li, L. Arnaud, P. Rockwell, and M.E. Figueiredo-Pereira A single amino acid substitution in a proteasome subunit triggers aggregation of ubiquitinated proteins in stressed neuronal cells J. Neurochem. 90 2004 19 28
8. R.K. Monroe, and S.W. Halvorsen Cadmium blocks receptor-mediated Jak/STAT signaling in neurons by oxidative stress Free Radic. Biol. Med. 41 2006 493 502
9. B. Okuda, Y. Iwamoto, H. Tachibana, and M. Sugita Parkinsonism after acute cadmium poisoning Clin. Neurol. Neurosurg. 99 1997 263 265
10. A.E. Panayi, N.M. Spyrou, B.S. Iversen, M.A. White, and P. Part Determination of cadmium and zinc in Alzheimers brain tissue using inductively coupled plasma mass spectrometry J. Neurol. Sci. 195 2002 1 10
11. M.E. Figueiredo-Pereira, S. Yakushin, and G. Cohen Disruption of the intracellular sulfhydryl homeostasis by cadmium-induced oxidative stress leads to protein thiolation and ubiquitination in neuronal cells J. Biol. Chem. 273 1998 12703 12709
12. E. Stadtman Protein oxidation and aging Science 257 1992 1220 1224
13. S.J. Stohs, and D. Bagchi Oxidative mechanisms in the toxicity of metal ions Free Radic. Biol. Med. 18 1995 321 336
14. 2+ currents: involvement of ROS and NF-kappaB J. Neurochem. 81 2002 1043 1051
15. L. Chen, L. Liu, and S. Huang 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 2008 1035 1044
16. P. Rockwell, J. Martinez, L. Papa, and E. Gomes Redox regulates COX-2 upregulation and cell death in the neuronal response to cadmium Cell. Signal. 16 2004 343 353
17. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 2007 245 313
18. J.D. Lambeth Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy Free Radic. Biol. Med. 43 2007 332 347
19. P. Polak, and M.N. Hall mTOR and the control of whole body metabolism Curr. Opin. Cell Biol. 21 2009 209 218
20. S. Huang, and P.J. Houghton Targeting mTOR signaling for cancer therapy Curr. Opin. Pharmacol. 3 2003 371 377
21. X. Gao, Y. Zhang, P. Arrazola, O. Hino, T. Kobayashi, R.S. Yeung, B. Ru, and D. Pan Tsc tumour suppressor proteins antagonize amino-acid-TOR signalling Nat. Cell Biol. 4 2002 699 704
22. K. Inoki, Y. Li, T. Zhu, J. Wu, and K.L. Guan TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling Nat. Cell Biol. 4 2002 648 657
23. A.R. Tee, D.C. Fingar, B.D. Manning, D.J. Kwiatkowski, L.C. Cantley, and J. Blenis Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling Proc. Natl Acad. Sci. USA 99 2002 13571 13576
24. H. Stocker, T. Radimerski, B. Schindelholz, F. Wittwer, P. Belawat, P. Daram, S. Breuer, G. Thomas, and E. Hafen Rheb is an essential regulator of S6K in controlling cell growth in Drosophila Nat. Cell Biol. 5 2002 559 565
25. Y. Zhang, X. Gao, L.J. Saucedo, B. Ru, B.A. Edgar, and D. Pan Rheb is a direct target of the tuberous sclerosis tumour suppressor proteins Nat. Cell Biol. 5 2003 578 581
26. A. Garami, F.J. Zwartkruis, T. Nobukuni, M. Joaquin, M. Roccio, H. Stocker, S.C. Kozma, E. Hafen, J.L. Bos, and G. Thomas Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2 Mol. Cell 11 2003 1457 1466
27. K. Inoki, Y. Li, T. Xu, and K.L. Guan Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling Genes Dev. 17 2003 1829 1834
28. A.R. Tee, B.D. Manning, P.P. Roux, L.C. Cantley, and J. Blenis Tuberous sclerosis complex gene products, tuberin and hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb Curr. Biol. 13 2003 1259 1268
29. X. Bai, D. Ma, A. Liu, X. Shen, Q.J. Wang, Y. Liu, and Y. Jiang Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38 Science 318 2007 977 980
30. X. Wang, B.D. Fonseca, H. Tang, R. Liu, A. Elia, M.J. Clemens, U.A. Bommer, and C.G. Proud Re-evaluating the roles of proposed modulators of mammalian target of rapamycin complex 1 (mTORC1) signaling J. Biol. Chem. 283 2008 30482 30492
31. M.N. Corradetti, K. Inoki, N. Bardeesy, R.A. DePinho, and K.L. Guan Regulation of the TSC pathway by LKB1: evidence of a molecular link between tuberous sclerosis complex and Peutz-Jeghers syndrome Genes Dev. 18 2004 1533 1538
32. A. Lau, J. Zhang, and J. Chiu Acquired tolerance in cadmium-adapted lung epithelial cells: roles of the c-Jun N-terminal kinase signaling pathway and basal level of metallothionein Toxicol. Appl. Pharmacol. 215 2006 1 8
33. E. Lopez, S. Figueroa, and M. Oset-Gasque M.P., G. Apoptosis and necrosis: two distinct events induced by cadmium in cortical neurons in culture Br. J. Pharmacol. 138 2003 901 911
34. L. Chen, L. Liu, Y. Luo, and S. Huang MAPK and mTOR pathways are involved in cadmium-induced neuronal apoptosis J. Neurochem. 105 2008 251 261
35. C.M. Findley, M.J. Cudmore, A. Ahmed, and C.D. Kontos VEGF induces Tie2 shedding via a phosphoinositide 3-kinase/Akt dependent pathway to modulate Tie2 signaling Arterioscler. Thromb. Vasc. Biol. 27 2007 2619 2626
36. L. Liu, L. Chen, J. Chung, and S. Huang Rapamycin inhibits F-actin reorganization and phosphorylation of focal adhesion proteins Oncogene 27 2008 4998 5010
37. T. Maehama, and J.E. Dixon The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3, 4, 5-trisphosphate J. Biol. Chem. 273 1998 13375 13378
38. Y. Zhu, P. Hoell, B. Ahlemeyer, and J. Krieglstein PTEN: a crucial mediator of mitochondria-dependent apoptosis Apoptosis 11 2006 197 207
39. Y. Zhu, P. Hoell, B. Ahlemeyer, U. Sure, H. Bertalanffy, and J. Krieglstein Implication of PTEN in production of reactive oxygen species and neuronal death in in vitro models of stroke and Parkinsons disease Neurochem. Int. 50 2007 507 516
40. D.D. Sarbassov, and D.M. Sabatini Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex J. Biol. Chem. 280 2005 39505 39509
41. L. Zhang, S.R. Kimball, L.S. Jefferson, and J.S. Shenberger Hydrogen peroxide impairs insulin-stimulated assembly of mTORC1 Free Radic. Biol. Med. 46 2009 1500 1509
42. L. Chen, B. Xu, L. Liu, Y. Luo, J. Yin, H. Zhou, W. Chen, T. Shen, X. Han, and S. Huang Hydrogen peroxide inhibits mTOR signaling by activation of AMPKalpha leading to apoptosis of neuronal cells Lab. Invest. 90 2010 762 773
43. R.S. Frey, M. Ushio-Fukai, and A. Malik NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology Antioxid. Redox Signaling 11 2009 791 810
44. A. Fujimoto, S. Akifusa, N. Kamio, T. Hirofuji, K. Nonaka, and Y. Yamashita Involvement of mTOR in globular adiponectin-induced generation of reactive oxygen species Free Radic. Res. 44 2010 128 134
45. D. Trachootham, J. Alexandre, and P. Huang Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discovery 8 2009 579 591
46. N.R. Leslie, D. Bennett, Y.E. Lindsay, H. Stewart, A. Gray, and C.P. Downes Redox regulation of PI 3-kinase signalling via inactivation of PTEN EMBO J. 22 2003 5501 5510
47. Y.D. Kwak, B. Wang, W. Pan, H. Xu, X. Jiang, and F.F. Liao Functional interaction of phosphatase and tensin homologue (PTEN) with the E3 ligase NEDD4-1 during neuronal response to zinc J. Biol. Chem. 285 2010 9847 9857
48. S. Fogarty, and D.G. Hardie Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer Biochim. Biophys. Acta 1804 2010 581 591
49. C. Culmsee, J. Monnig, B.E. Kemp, and M.P. Mattson AMP-activated protein kinase is highly expressed in neurons in the developing rat brain and promotes neuronal survival following glucose deprivation J. Mol. Neurosci. 17 2001 45 58
50. B. Dasgupta, and J. Milbrandt Resveratrol stimulates AMP kinase activity in neurons Proc. Natl Acad. Sci. USA 104 2007 7217 7222