Cadmium-induced apoptotic death of human retinal pigment epithelial cells is mediated by MAPK pathway

Experimental Eye Research

Volumn 89, Issue 4, 2009, Pages 494-502

  Kalariya, Nilesh M ^a   Wills, Nancy K ^a   Ramana, Kota V ^a   Srivastava, Satish K ^a   van Kuijk, Frederik J G M ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

AMD; apoptosis; cadmium; MAPK; oxidative stress; retinal pigment epithelium

Indexed keywords

ACETYLCYSTEINE; BUTHIONINE SULFOXIMINE; CADMIUM; CIGARETTE SMOKE; CYTOCHROME C; GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL VIABILITY; CIGARETTE SMOKING; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME RELEASE; EPITHELIUM CELL; HUMAN; HUMAN CELL; INDUSTRIAL WASTE; METAL INDUSTRY; MITOCHONDRIAL MEMBRANE POTENTIAL; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; SIGNAL TRANSDUCTION; TIME; TOXICOKINETICS;

ACETYLCYSTEINE; APOPTOSIS; BLOTTING, WESTERN; BUTHIONINE SULFOXIMINE; CADMIUM CHLORIDE; CELL LINE; CELL SURVIVAL; CYTOCHROMES C; CYTOSOL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FLOW CYTOMETRY; GLUTATHIONE; HUMANS; HYDROGEN PEROXIDE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; RETINAL PIGMENT EPITHELIUM; TIME FACTORS;

EID: 69749099385     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2009.05.011     Document Type: Article

References (54)

1. Arisawa K., Uemura H., Hiyoshi M., Takeda H., Saito H., and Soda M. Cadmium-induced renal dysfunction and mortality in two cohorts: disappearance of the association in a generation born later. Toxicol. Lett. 169 3 (2007) 214-221
2. Baker J.R., Edwards R.J., Lasker J.M., Moore M.R., and Satarug S. Renal and hepatic accumulation of cadmium and lead in the expression of CYP4F2 and CYP2E1. Toxicol. Lett. 159 (2005) 182-191
3. Bertin G., and Averbeck D. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences. Biochimie 88 11 (2006) 1549-1559
4. Bhattacharyya M.H., Wilson A.K., Rajan S.S., and Jonah M. Biochemical pathways in cadmium toxicity. In: Zalups R.R., and Koropatrick J. (Eds). Molecular Biology and Toxicology of Metals (2000), Taylor and Francis, London 2000
5. Cao Z., Hardej D., Trombetta L.D., and Li Y. The role of chemically induced glutathione and glutathione S-transferase in protecting against 4-hydroxy-2-nonenal-mediated cytotoxicity in vascular smooth muscle cells. Cardiovasc. Toxicol. 3 2 (2003) 165-177
6. Chen L., Liu L., Luo Y., and Huang S. MAPK and mTOR pathways are involved in cadmium-induced neuronal apoptosis. J. Neurochem. 105 (2008) 251-261
7. Chen L., Liu L., and Huang S. 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
8. Chuang S.M., Wang I.C., and Yang J.L. Roles of JNK, p38 and ERK mitogen-activated protein kinases in the growth inhibition and apoptosis induced by cadmium. Carcinogenesis 21 (2000) 1423-1432
9. Erie J.C., Butz J.A., Good J.A., Erie E.A., Burritt M.F., and Cameron J.D. Heavy metal concentrations in human eyes. Am. J. Ophthalmol. 139 5 (2005) 888-893
10. Erie J.C., Good J.A., Butz J., Hodge D.O., and Pulido J.S. Urinary cadmium and age related macular degeneration. Am. J. Ophthalmol. 144 3 (2007) 414-418
11. Friberg L. Cadmium. Annu. Rev. Public Health 4 (1983) 367-373
12. Fritsche L.G., Loenhardt T., Janssen A., Fisher S.A., Rivera A., et al. Age-related macular degeneration is associated with an unstable ARMS2 (LOC387715) mRNA. Nat. Genet. 40 (2008) 892-896
13. Fujihara M., Nagai N., Sussan T.E., Biswal S., and Handa J.T. Chronic cigarette smoke causes oxidative damage and apoptosis to retinal pigmented epithelial cells in mice. PLoS ONE 3 (2008) e3119
14. Gallagher C.M., Kovach J.S., and Meliker J.R. Urinary cadmium and osteoporosis in U.S. Women > or = 50 years of age: NHANES. Environ. Health Perspect. 116 10 (2008) 1338-1343
15. Glotin A., Calipel A., Brossas J., Faussat A., Treton J., and Mascarelli F. Sustained versus transient Erk1/2 signalling underlies the anti- and proapoptotic effects of oxidative stress in human RPE cells. Invest. Ophthalmol. Vis. Sci. 47 10 (2006) 4614-4623
16. He L., Girijashanker K., Dalton T.P., Reed J., Li H., Soleimani M., and Nebert D.W. ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol. Pharmacol. 70 (2006) 171-180
17. Ho T.C., Yang Y.C., Cheng H.C., Wu A.C., Chen S.L., Chen H.K., and Tsao Y.P. Activation of mitogen-activated protein kinases is essential for hydrogen peroxide-induced apoptosis in retinal pigment epithelial cells. Apoptosis 11 (2006) 1899-1908
18. Hollyfield J.G., Bonilha V.L., Rayborn M.E., Yang X., Shadrach K.G., Lu L., Ufret R.L., Salomon R.G., and Perez V.L. Oxidative damage-induced inflammation initiates age related macular degeneration. Nat. Med. 14 2 (2008) 194-198
19. Horiguchi H. Anemia induced by cadmium intoxication. Nippon Eiseigaku Zasshi 62 3 (2007) 888-904
20. Houston M.C. The role of mercury and cadmium heavy metals in vascular disease, hypertension, coronary heart disease, and myocardial infarction. Altern. Ther. Health Med. 13 2 (2007) 128-133
21. Johnson S. Gradual micronutrient accumulation and depletion in Alzheimer's disease. Med. Hypotheses 56 (2001) 595-597
22. Jung Y.S., Jeong E.M., Park E.K., Kim Y.M., Sohn S., Lee S.H., Baik E.J., and Moon C.H. Cadmium induces apoptotic cell death through p38 MAPK in brain microvessel endothelial cells. Eur. J. Pharmacol. 578 1 (2008) 11-18
23. Kalariya N.M., Ramana K.V., Srivastava S.K., and van Kuijk F.J. Carotenoid derived aldehydes-induced oxidative stress causes apoptotic cell death in human retinal pigment epithelial cells. Exp. Eye Res. 86 1 (2008) 70-80
24. Kim S., Moon C., Eun S., Ryu P., and Jo S. 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
25. Klein R., Knudtson M.D., Cruickshanks K.J., and Klein B.E. Further observations on the association between smoking and the long-term incidence and progression of age-related macular degeneration: the Beaver Dam Eye Study. Arch. Ophthalmol. 126 1 (2008) 115-121
26. Kukner A., Colakoglu N., Kara H., Oner H., Ozogul C., and Ozan E. Ultrastructural changes in the kidney of rats with acute exposure to cadmium and effects of exogenous metallothionein. Biol. Trace Elem. Res. 119 2 (2007) 137-146
27. Lag M., Refsnes M., Lilleaas E.M., Holme J.A., Becher R., and Schwarze P.E. Role of mitogen activated protein kinases and protein kinase C in cadmium-induced apoptosis of primary epithelial lung cells. Toxicology 211 3 (2005) 253-264
28. Lei Y.X., Wei L., Wang M., Wu G.R., and Li M. Malignant transformation and abnormal expression of eukaryotic initiation factor in bronchial epithelial cells induced by cadmium chloride. Biomed. Environ. Sci. 21 4 (2008) 332-338
29. Li Z., Arnaud L., Rockwell P., and Figueiredo-Pereira M.E. A single amino acid substitution in a proteasome subunit triggers aggregation of ubiquitinated proteins in stressed neuronal cells. J. Neurochem. 90 (2004) 19-28
30. Liles M.R., Newsome D.A., and Oliver P.D. Antioxidant enzymes in the aging human retinal pigment epithelium. Arch. Ophthalmol. 109 9 (1991) 1285-1288
31. Lopez E., Figueroa S., Oset-Gasque M., and Gonzalez M.P. Apoptosis and necrosis: two distinct events induced by cadmium in cortical neurons in culture. Br. J. Pharmacol. 138 (2003) 901-911
32. Mannino D.M., Holguin F., Greves H.M., Savage-Brown A., Stock A.L., and Jones R.L. Urinary cadmium levels predict lower lung function in current and former smokers: data from the Third National Health and Nutrition Examination Survey. Thorax 59 3 (2004) 194-198
33. Martin P., Poggi M.C., Chambard J.C., Boulukos K.E., and Pognonec P. Low dose cadmium poisoning results in sustained ERK phosphorylation and caspase activation. Biochem. Biophys. Res. Commun. 350 3 (2006) 803-807
34. Meister A., Anderson M.E., and Hwang O. Intracellular cysteine and glutathione delivery systems. J. Am. Coll. Nutr. 5 (1986) 137-151
35. Monroe R.K., and Halvorsen S.W. Cadmium blocks receptor-mediated Jak/STAT signaling in neurons by oxidative stress. Free Radic. Biol. Med. 41 (2006) 493-502
36. Nordberg G.F., Nogawa K., Nordberg M., and Friberg L.T. Cadmium. In: Aitio A., Andersson I., Fowler B.A., Friberg L.T., Nordberg G.F., Nordberg M., Part P., and Skerfving S. (Eds). Handbook on the Toxicology of Metals (2007), Elsevier, Amsterdam 445-486 2007
37. Okuda B., Iwamoto Y., Tachibana H., and Sugita M. Parkinsonism after acute cadmium poisoning. Clin. Neurol. Neurosurg. 99 (1997) 263-265
38. Prozialeck W.C., Vaidya V.S., Liu J., Waalkes M.P., Edwards J.R., Lamar P.C., Bernard A.M., Dumont X., and Bonventre J.V. Kidney injury molecule-1 is an early biomarker of cadmium nephrotoxicity. Kidney Int. 72 8 (2007) 985-993
39. Ramana K.V., Bhatnagar A., Srivastava S., Yadav U.C., Awasthi S., Awasthi Y.C., and Srivastava S.K. Mitogenic responses of vascular smooth muscle cells to lipid peroxidation-derived aldehyde 4-hydroxy-trans-2-nonenal (HNE): role of aldose reductase-catalyzed reduction of the HNE-glutathione conjugates in regulating cell growth. J. Biol. Chem. 281 26 (2006) 17652-17660
40. Rivera A., Fisher S.A., Fritsche L.G., Keilhauer C.N., Lichtner P., et al. Hypothetical LOC387715 is a second major susceptibility gene for age-related macular degeneration, contributing independently of complement factor H to disease risk. Hum. Mol. Genet. 14 (2005) 3227-3236
41. Rockwell P., Martinez J., Papa L., and Gomes E. Redox regulates COX-2 upregulation and cell death in the neuronal response to cadmium. Cell. Signal. 16 (2004) 343-353
42. Satarug S., and Moore M.R. Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environ. Health Perspect. 112 10 (2004) 1099-1103
43. Satarug S., Ujjin P., Vanavanitkun Y., Baker J.R., and Moore M.R. Influence of body iron store status and cigarette smoking on cadmium body burden of healthy Thai women and men. Toxicol. Lett. 148 3 (2004) 177-185
44. Satarug S., Kikuchi M., Wisedpanichkij R., Li B., Takeda K., Na-Bangchang K., Moore M.R., Hirayama K., and Shibahara S. Prevention of cadmium accumulation in retinal pigment epithelium with manganese and zinc. Exp. Eye Res. 87 6 (2008) 587-593
45. Schmidt S., Hauser M.A., Scott W.K., Postel E.A., Agarwal A., et al. Cigarette smoking strongly modifies the association of LOC387715 and age-related macular degeneration. Am. J. Hum. Genet. 78 (2006) 852-864
46. Singh K.P., Kumari R., Pevey C., Jackson D., and Dumond J.W. Long duration exposure to cadmium leads to increased cell survival, decreased DNA repair capacity, and genomic instability in mouse testicular Leydig cells. Cancer Lett. 279 1 (2009) 84-92
47. Srivastava S.K., and Beutler E. The transport of oxidized glutathione from the erythrocytes of various species in the presence of chromate. Biochem. J. 114 (1969) 833-837
48. Thijssen S., Lambrichts I., Maringwa J., and Van Kerkhove E. Changes in expression of fibrotic markers and histopathological alterations in kidneys of mice chronically exposed to low and high Cd doses. Toxicology 238 2-3 (2007) 200-210
49. Wang A.L., Lukas T.J., Yuan M., Du N., Handa J.T., and Neufeld A.H. Changes in retinal pigment epithelium related to cigarette smoke: possible relevance to smoking as a risk factor for age-related macular degeneration. PLoS ONE 4 4 (2009) e5304
50. Wills N.K., Sadagopa Ramanujam V.M., Chang-Strepka J., Kalariya N., Lewis J.R., and van Kuijk F.J. Cadmium accumulation in the aging human retina. Exp. Eye Res. 86 1 (2008) 41-51
51. Wills N.K., Sadagopa Ramanujam V.M., Kalariya N., Lewis J.R., and van Kuijk F.J.M. Copper and zinc distribution in the human retina: relationship to cadmium accumulation, age, and gender. Exp. Eye Res. 87 2 (2008) 80-88
52. Wills N.K., Kalariya N., Sadagopa Ramanujam V.M., Lewis J.R., Haji Abdollahi S., Husain A., and van Kuijk F.J. Human retinal cadmium accumulation as a factor in etiology of age-related macular degeneration. Exp. Eye Res. 89 1 (2009) 79-87
53. Yadav U.C., Ramana K.V., Awasthi Y.C., and Srivastava S.K. Glutathione level regulates HNE-induced genotoxicity in human erythroleukemia cells. Toxicol. Appl. Pharmacol. 227 2 (2008) 257-264
54. Zarbin M.A. Current concepts in the pathogenesis of age-related macular degeneration. Arch. Ophthalmol. 122 4 (2004) 598-614