Effects of thimerosal on NGF signal transduction and cell death in neuroblastoma cells

Toxicological Sciences

Volumn 86, Issue 1, 2005, Pages 132-140

  Parran, Damani K ^a   Barker, Angela ^a   Ehrich, Marion ^a  

^a VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

Author keywords

Mercury compound; Neurotrophin; Signal transduction

Indexed keywords

DNA FRAGMENT; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; PROTEIN KINASE C DELTA; PROTEIN TYROSINE KINASE A; THIOMERSAL; PRKCD PROTEIN, HUMAN; PROTEIN KINASE C;

APOPTOSIS; ARTICLE; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; NERVE CELL NECROSIS; NEUROBLASTOMA CELL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; DRUG EFFECT; ENZYMOLOGY; METABOLISM; NEUROBLASTOMA; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

CELL DEATH; CELL LINE, TUMOR; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE GROWTH FACTOR; NEUROBLASTOMA; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-DELTA; SIGNAL TRANSDUCTION; THIMEROSAL;

EID: 26944493075     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfi175     Document Type: Article

References (77)

1. Abemayor, E., and Sidell, N. (1989). Human neuroblastoma cell lines as models for the in vitro study of neoplastic and neuronal cell differentiation. Environ. Health Perspect. 80, 3-15.
2. Alexandre, H., Delsinne, V., Goval, J. J., and Van Cauwenberge, A. (2003). Effect of taxol and okadaic acid on microtubule dynamics in thimerosal-arrested primary mouse oocytes: A confocal study. Biol. Cell 95, 407-414.
3. Barde, Y.-A. (1989). Trophic factors and neuronal survival: Review. Neuron 2, 1525-1534.
4. Baskin, D. S., Ngo, H., and Didenko, V. V. (2003). Thimerosal induces DNA breaks, caspase-3 activation, membrane damage and cell death in cultured human neurons and fibroblasts. Toxicol. Sci. 74, 361-368.
5. Batistatou, A., and Greene, L. A. (1993). Internucleosomal DNA cleavage and neuronal cell survival/death. J. Cell Biol. 122, 523-532.
6. Bernard, S., Enayati, A., Roger, H., Binstock, T., and Redwood, L. (2001). The role of mercury in the pathogenesis of autism. Mol. Psychiatry 7, S42-S43.
7. Blair, A., Clark, B., Clarke, A., and Wood, P. (1975). Tissue concentrations of mercury after chronic dosing of squirrel monkeys with thimerosal. Toxicology 3, 171-176.
8. Brodie, C., Bogi, K., Acs, P., Lazarovici, P., Petrovics, G., Anderson, W. B., and Blumberg, P. M. (1999). Protein kinase C-ε plays a role in neurite outgrowth in response to epidermal growth factor and nerve growth factor in PC12 Cells. Cell Growth Differ. 10, 183-191.
9. Castoldi, A. F., Barni, S., Turin, I., Gandini, C., and Manzo, L. (2000). Early acute necrosis, delayed apoptosis and cytoskeletal breakdown in cultured cerebellar granule neurons exposed to methylmercury. J. Neurosci. Res. 59, 775-787.
10. Choi, Y. B., and Lipton, S. A. (2000). Redox modulation of the NMDA receptor. Cell. Mol. Life Sci. 57, 1535-1541.
11. Corbit, K. C., Foster, D. A., and Rosner, M. R. (1999). Protein kinase C-delta mediates neurogenic but not mitogenic activation of mitogen-activated protein kinase in neuronal cells. Mol. Cell. Biol. 19(6), 4209-4218.
12. Corbit, K. C., Soh, J. W., Yoshida, K., Eves, E. M., Weinstein, I. B., and Rosner, M. R. (2000). Different protein kinase C isoforms determine growth factor specificity in neuronal cells. Mol. Cell. Biol. 20, 5392-5403.
13. Dey, P. M., Gochfeld, M., and Reuld, K. R. (1999) Developmental methylmercury administration alters cerebellar PSA-NCAM expression and Golgi sialyltransferase activity. Brain Res. 845, 139-151.
14. Dikic, I., Schlessinger, J., and Lax, I. (1994). PC12 cells overexpressing the insulin receptor undergo insulin-dependent neuronal differentiation. Curr. Biol. 4, 702-708.
15. Eggert, A., Ikegaki, N., Liu, X.-G., Chou, T. T., and Brodeur, G. M. (2001). TrkA signal transduction pathways in neuroblastoma. Med. Pediatr. Oncol. 36, 108-110.
16. Fagerstrom, S., Pahlman, S., Gestblom, C., and Nanberg, E. (1996). Protein kinase C-epsilon is implicated in neurite outgrowth in differentiating human neuroblastoma cells. Cell Growth & Differ 7, 775-785.
17. Fujita, K., Lazarovici, P., and Guroff, G. (1989). Regulation of the differentiation of PC pheochromocytoma cells. Environ. Health Perspect. 80, 127-142.
18. Gonzalez, E. A., Seth, A., Raden, D. L., Bowman, D. S., Fay, E S., and Davis, R. J. (1993). Serum-induced translocation of mitogen-activated protein kinase to the cell surface ruffling membrane and the nucleus. J. Cell Biol. 122, 1089-1101.
19. Graff, R. D., Falconer, M. M., Brown, D. L., and Reuld, K. R. (1997). Altered sensitivity of posttranslationally modified microtubules to methylmercury in differentiating embryonal carcinoma-derived neurons. Toxicol. Appl. Pharmacol. 144, 215-224.
20. Greene, L. A., and Kaplan, D. R. (1995). Early events in neurotrophin signalling via trk and p75 receptors. Curr. Opinion Neurobiol. 5, 579-587.
21. Gryz, E. A., and Meakin, S. O. (2003). Acidic substitution of the activation loop tyrosines in TrkA supports nerve growth factor-dependent, but not nerve growth factor-independent differentation and cell cycle arrest in the human neuroblastoma cell line, SY5Y. Oncogene 22, 8774-8785.
22. Hampton, M. B., and Orrenius, S. (1998). Redox regulation of apoptotic cell death in the immune system. Toxicol. Lett. 102-103, 355-358.
23. Heidemann, S. R., Joshi, H. C., Schechter, A., Fletcher, J. R., and Bothwell, M. (1985). Synergistic effects of cyclic AMP and nerve growth factor on neurite outgrowth and microtubule stability of PC12 cells. J. Cell Biol. 100, 916-927.
24. Inoue, Y., Saijoh, K., and Sumino, K. (1988). Action of mercurials on activity of partially purified soluble protein kinase C from mice brain. Pharmacol. Toxicol. 62, 278-281.
25. Jackson, G. R., Apffel, L., Werrbach-Perez, K., and Perez-Polo, J. R. (1990). Role of nerve-growth factor in oxidant-antioxidant balance and neuronal injury: I. Stimulation of hydrogen peroxide resistance. J. Neurosci. Res. 25, 360-368.
26. James, S. J., Slikker, W., Melnyk, S., New, E., Pogribna, M., and Jernigan, S. (2005). Thimerosal neurotoxicity is associated with glutathione depletion: Protection with glutathione precursors. Neurotoxicology 26, 1-8.
27. Kao, S., Jaiswal, R. K., Kolch, W., and Landreth, G. E. (2001). Identification of the mechanisms regulating the differential activation of the MAPK cascade by epidermal growth factor and nerve growth factor in PC12 cells. J. Biol. Chem. 276, 18169-18177.
28. Kaplan, D. R., Hempstead, B. L., Martin-Zanca, D., Chao, M. V., and Parada, L. F. (1991). The trk proto-oncogen product: A signal transducing receptor for nerve growth factor. Science 252, 554-558.
29. Kaplan, D. R., and Miller, F. D. (1997). Signal transduction by the neurotrophin receptors. Curr. Opinion Cell Biol. 9, 213-221.
30. Kidd, P. M. (2002). Autism, an extreme challenge to integrative medicine. Part 1: The knowledge base. Alternative Med. Rev. 7, 292-316.
31. Kiley, S. C., Welsh, J., Narvaez, C. J., and Jaken, S. (1996). Protein kinase C isozymes and substrates in mammary carcinogenesis. J. Mammary Gland Biol. Neoplasia 1, 177-187.
32. Lagunowich, L. A., and Grunwald, G. B. (1991) Tissue and age-specificity of post-translational modifications of N- cadherin during chick embryo development. Differentiation 47, 19-27.
33. Lavenius, E., Parrow, V., Nanberg, E., and Pahlman, S. (1994). Basic FGF and IGF-1 promote differentiation of human SH-SY5Y neuroblastoma cells in culture. Growth Factors 10, 29-39.
34. Loeb, D. M., and Greene, L. A. (1993). Transfection with trk restores "slow" NGF binding, efficient NGF uptake, and multiple NGF responses to NGF-nonresponsive PC12 cell mutants. J. Neurosci. 13, 2919-2929.
35. Macho, A., Hirsch, T., Marzo, I., Marchetti, P., Dallaporta, B., Susin, S. A., Zamzami, N., and Kroemer, G. (1997). Glutathione depletion is an early and calcium elevation is a late event of thymocyte apoptosis. J. Immunol. 158(10), 4612-4619.
36. Magos, L. (2001). Review on the toxicity of ethylmercury, including its presence as a preservative in biological and pharmaceutical products. J. Appl. Toxicol. 21, 1-5.
37. Magos, L. (2003). Neurotoxic character of thimerosal and the allometric extrapolation of adult clearance half-time to infants. J. Appl. Toxicol. 23, 263-269.
38. Magos, L., Brown, A. W., Sparrow, S., Bailey, E., Snowden, R. T., and Skipp, W. R. (1985). The comparative toxicology of ethyl- and methylmercury. Arch. Toxicol. 57, 260-267.
39. Makani, S., Gollapudi, S., Yel, L., Chiplunkar, S., and Gupta, S. (2002). Biochemical and molecular basis of thimerosal-induced apoptosis in T-cells: Major role of mitochondrial pathway. Genes Immun. 3, 270-278.
40. Marshall, C. J. (1995). Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
41. Martin-Zanca, D., Oskam, R., Mitra, G., Copeland, T. D., and Barbacid, M. (1989). Molecular and biochemical characterization of the human trk proto-oncogen. Mol. Cell. Biol. 9, 24-33.
42. Mates, J. M., Perez-Gomez, C., Nunez de Castro, I., Asenjo, M., and Marquez, J. (2002). Glutamine and its relationship with intracellular redox status, oxidative stress and cell proliferation/death. Int. J. Biochem. Cell Biol. 31, 697-703.
43. Meister, A. (1995). Glutathione metabolism. Methods Enzymol. 251, 3-7.
44. Nakagawara, A., Arima-Nakagawara, M., Scavarda, N. J., Azar, C. G., Cantor, A. B., and Brodeur, G. M. (1993). Association between high levels of expression of the TRK gene and favorable outcome in human neuroblastoma. New Engl. J. Med. 328, 847-854.
45. National Academy of Sciences. Link between neurodevelopmental disorders and thimerosal remains unclear. http://www4.nationalacademies.org/ news.nsf/isbn/0309076366?OpenDocument.
46. O'Driscoll, K. R., Teng, K. K., Fabbro, D., Greene, L. A., and Weinstein. (1995). Selective translocation of protein kinase C-delta in PC12 cells during nerve growth factor-induced neuritogenesis. Mol. Cell. Biol. 6, 449-458.
47. Ou, Y. C., Thompson, S. A., Kirchner, S.C., Kavanagh, T. J., and Faustman, E. M. (1997). Induction of growth arrest and DNA damage-inducible genes Gadd45 and Gadd153 in primary rodent embryonic cells following exposure to methylmercury. Toxicol. Appl. Pharmacol. 147, 31-38.
48. Pang, L., Zheng, C. F., Guan, K. L., and Saltiel, A. R. (1995). Nerve growth factor stimulates a novel protein kinase in PC-12 cells that phosphorylates and activates mitogen-activated protein kinase kinase (MEK). Biochem. J. 307, 513-519.
49. Parran, D. K., Mundy, W. R., and Barone, S. (2001). Effects of methylmercury and mercuric chloride on differentiation and cell viability in PC12 cells. Toxicol. Sci. 59(2), 278-290.
50. Parran, D. K., Barone, S., and Mundy, W. R. (2003). Methylmercury decrease NGF-induced TrkA autophosphorylation and neurite outgrowth in PC12 cells. Dev. Brain Res. 141(1-2), 71-81.
51. Parran, D. K., Barone, J., S, and Mundy, W. R. (2004). Methylmercury inhibits TrkA signaling through the ERK1/2 cascade after NGF stimulation of PC12 cells. Dev. Brain Res. 149, 53-61.
52. Parrow, V., Fagerstrom, S., Meyerson, G., Nanberg, E., and Pahlman, S. (1995). Protein kinase C-alpha and -epsilon are enriched in growth cones of differentiating SH-SY5Y human neuroblastoma cells. J. Neurosci. Res. 41, 782-791.
53. Peraus, G. C., Masters, C. L., and Beyreuther, K. (1997). Late compartments of amyloid precursor protein transport in SY5Y cells are involved in beta-amyloid secretion. J. Neurosci. 17, 7714-7724.
54. Pessah, I. N. (2001). Ryanodine receptor acts as a sensor for redox stress. Pest Manage. Sci. 57, 941-945.
55. Pittman, R. N., Wang, S., Dibenedetto, A. J., and Mills, J. C. (1993). A system for characterizing cellular and moleculer events in programmed cell death. J. Neurosci. 13, 3669-3680.
56. Ponce, R. A., Kavanagh, T. J., Monet, N. K., Whittaker, S. G., and Faustman, E. M. (1994). Effects of methyl mercury on the cell cycle of primary rat CNS cells in vitro. Toxicol. Appl. Pharmacol. 127, 83-90.
57. Qiu, M. S., and Green, S. H. (1991). NGF and EGF rapidly activate p21ras in PC12 cells by distinct, convergent pathways involving tyrosine phosphorylation. Neuron 7, 937-946.
58. Rabizadeh, S., Oh, J., Zhong, L. T., Yang, J., Bider, C. M., Butcher, L. L., and Bredesen, D. E. (1993). Induction of apoptosis by the low-afinity NGF receptor. Science 261, 345-348.
59. Sanfeliu, C., Sebastia, J., and Ki, S. U. (2001). Methylmercury neurotoxicity in cultures of human neurons, astrocytes, neuroblastoma cells. Neurotoxicology 22(3), 317-327.
60. Segal, R. A., Goumnerova, L. C., Kwon, Y. K., Stiles, C. D., and Pomeroy, S. L. (1994). Expression of the neurotrophin receptor TrkC is linked to a favorable outcome in medulloblastoma. Proc. Natl. Acad. Sci. 91, 12867-12871.
61. + induced apoptotic cell death in SH-SY5Y neuroblastoma cells: An electron microscope study. J. Neurosci. Res. 48, 226-237.
62. Soderholm, H., Olsson, A.-K., Lavenius, E., Ronnstrand, L., and Nanberg, E. (2001). Activation of Ras, Raf-1 and protein kinase C in differentiating human neuroblastoma cells after treatment with phorbolester and NGF. Cell. Signaling 13, 95-104.
63. Speizer, L. A., Watson, M. J., Kanter, J. R., and Brunton, L. L. (1989). Inhibition of phorbol ester binding and protein kinase C activity by heavy metals. J. Biol. Chem. 264, 5585-5587.
64. Stephens, R. M., Loeb, D. M., Copeland, T. D., Pawson, T., and Greene, L. A. (1994). Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma-1 to mediate NGF responses. Neuron 12, 691-705.
65. Suzuki, T. T. M., and Toyama, C. (1973). The chemical form and bodily distribution of mercury in marine fish. Bull. Environ. Contam. Toxicol. 10, 347-355.
66. Szeberenyi, J., and Erhardt, P. (1994). Cellular components of nerve growth factor signaling. Biochimica et Biophysica Acta 1222, 187-202.
67. Thoenen, H. (1991). The changing scene of neurotrophic factors. Trends Neurosci. 14, 165-170.
68. Traverse, S., Gomez, N., Paterson, H., Marshall, C., and Cohen, P. (1992). Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288, 351-355.
69. 2+ concentration of rat cerebellar neurons. Toxicology 195, 77-84.
70. Ueha-Ishibashi, T., Tatsuishi, T., Iwase, K., Nakao, H., Umebayashi, C., Nishizaki, Y., Nishimura, Y., Oyama, Y., Hirama, S., and Okano, Y. (2004b). Property of thimerosal-induced decrease in cellular content of glutathione in rat thymocytes: A flow cytometric study with 5-chloromethylfluorescein diacetate. Toxicol. In Vitro 18, 563-569.
71. Ulfvarson, U. (1962). Distribution and excretion of some mercury compounds after long term exposure. Internation Archives of Gewerbepathol Gewerbehyg 19, 412-422.
72. Vanlingen, S., Sipma, H., De Smet, P., Callewaert, G., Missiaen, L., De Smet, H., and Parys, J. B. (2001). Modulation of inositol 1,4,5-triphosphate binding to the various inositol 1,4,5-triphosphate receptor isoforms by thimerosal and cyclic ADP-ribose. Biochem. Pharmacol. 61, 803-809.
73. Wasteneys, G. O., Cadrin, M., Reuld, K. R., and Brown, D. L. (1988). The effects of methylmercury on the cytoskeleton of murine embryonal carcinoma cells. Cell. Biol. Toxicol. 4, 41-60.
74. Westphal, G. A., Asgari, S., Schulz, T. G., Bunger, J., Muller, M., and Hallier, E. (2003). Thimerosal induces micronuclei in the cytochalasin B block micronucleus test with human lymphocytes. Arch. Toxicol. 77, 50-55.
75. Wyllie, A. H. (1980). Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555-556.
76. Zeidman, R., Lofgren, B., Pahlman, S., and Larsson, C. (1999). PKC-epsilon via its regulatory domain and independently of its catalytic domain induces neurite-like processes in neuroblastoma cells. Journal of Cell Biology 145, 713-726.
77. Zhou, J., Valletta, J. S., Grimes, M. L., and Mobley, W. C. (1995). Multiple levels for regulation of TrkA in PC12 cells by nerve growth factor. J. Neurochem. 65, 1146-1156.