ERK activation and nuclear translocation in amyloid-β peptide- and iron-stressed neuronal cell cultures

European Journal of Neuroscience

Volumn 16, Issue 1, 2002, Pages 44-54

  Kuperstein, Faina ^a   Yavin, Ephraim ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Alzheimer's disease; Amyloid beta; Apoptosis; ERK; Iron; Neuronal cells; Oxidative stress

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ACETYLCYSTEINE; AMYLOID BETA PROTEIN; ANTIOXIDANT; CASPASE 3; CATALASE; CHELATING AGENT; DEFEROXAMINE; FLUORESCEIN DERIVATIVE; IRON; LIPID PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PEPTIDE FRAGMENT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; MITOCHONDRION; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; AMYLOID BETA-PROTEIN; ANIMALS; ANTIOXIDANTS; APOPTOSIS; BUTADIENES; CASPASE 3; CASPASES; CELL CULTURE TECHNIQUES; CELL NUCLEUS; CEREBRAL CORTEX; DEFEROXAMINE; ENZYME ACTIVATION; ENZYME INHIBITORS; IRON; IRON CHELATING AGENTS; LIPID PEROXIDATION; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; NITRILES; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PROTEIN TRANSPORT; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 0036458808     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02056.x     Document Type: Article

References (70)

1. Atwood, C.S., Huang, X., Moir, R.D., Tanzi, R.E. & Bush, A.I. (1999) Role of free radicals and metal ions in the pathogenesis of Alzheimer's disease. Metal. Ions Biol. Syst., 36, 309-364.
2. Atwood, C.S., Scarpa, R.C., Huang, X., Moir, R.D., Jones, W.D., Fairlie, D.P., Tanzi, R.E. & Bush, A.I. (2000) Characterization of copper interactions with alzheimer amyloid beta peptides, identification of an attomolar-affinity copper binding site on amyloid beta1-42. J. Neurochem., 75, 1219-1233.
3. Behl, C. (1997) Amyloid beta-protein toxicity and oxidative stress in Alzheimer's disease. Cell Tissue Res., 290, 471-480.
4. Behl, C. (2000) Apoptosis and Alzheimer's disease. J. Neural Transm., 107, 1325-1344.
5. Braak, H. & Braak, E. (1997) Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol. Aging, 18, 351-357.
6. Bradford, M.M. (1986) A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 238-259.
7. Brand, A., Gil, S. & Yavin, E. (2000) N-Methyl bases of ethanolamine prevent apoptotic cell death induced by oxidative stress in cells of oligodendroglia origin. J. Neurochem., 74, 1596-1604.
8. Brunet, A., Roux, D., Lenormand, P., Dowd, S., Keyse, S. & Pouyssegur, J. (1999) Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor- induced gene expression and cell cycle entry. EMBO J., 18, 664-674.
9. Chen, R.H., Sarnecki, C. & Blenis, J. (1992) Nuclear localization and regulation of ERK- and RSK-encoded protein kinases. Mol. Cell. Biol., 12, 915-927.
10. Chong, Y.H., Sung, J.H., Shin, S.A., Chung, J.H. & Suh, Y.H. (2002) Effects of the beta-amyloid and carboxyl-terminal fragment of Alzheimer's amyloid precursor protein on the production of tumor necrosis factor alpha and matrix metalloproteinase-9 by human monocytic THP-1. J. Biol. Chem, 276, 23511-23517.
11. Combs, C.K., Johnson, D.E., Cannady, S.B., Lehman, T.M. & Landreth, G.E. (1999) Identification of microglial signal transduction pathways mediating a neurotoxic response to amyloidogenic fragments of beta-amyloid and prion proteins. J. Neurosci., 19, 928-939.
12. Cotman, C.W. (1997) The beta-amyloid peptide, peptide self-assembly, and the emergence of biological activities. A new principle in peptide function and the induction of neuropathology. Ann. NY Acad. Sci., 814, 1-16.
13. Cuajungco, M.P., Faget, K.Y., Huang, X., Tanzi, R.E. & Bush, A.I. (2000) Metal chelation as a potential therapy for Alzheimer's disease. Ann. NY Acad. Sci., 920, 292-304.
14. Deuther-Conrad, W., Loske, C., Schinzel, R., Dringen, R., Riederer, P. & Munch, G. (2001) Advanced glycation endproducts change glutathione redox status in SH-SY5Y human neuroblastoma cells by a hydrogen peroxide dependent mechanism. Neurosci. Lett., 312, 29-32.
15. Estus, S., Tucker, H.M., van Rooyen, C., Wright, S., Brigham, E.F., Wogulis, M. & Rydel, R.E. (1997) Aggregated amyloid-beta protein induces cortical neuronal apoptosis and concomitant 'apoptotic' pattern of gene induction. J. Neurosci., 17, 7736-7745.
16. Furuno, T., Hirashima, N., Onizawa, S., Sagiya, N. & Nakanishi, M. (2001) Nuclear shuttling of mitogen-activated protein (map) kinase (extracellular signal-regulated kinase (erk) 2) was dynamically controlled by map/erk kinase after antigen stimulation in rbl-2h3 cells. J. Immunol., 166, 4416- 4421.
17. Gerlach, M., Ben-Shachar, D. & Riederer, P. (1994) and Youdim MB. Altered brain metabolism of iron as a cause of neurodegenerative diseases? J. Neurochem., 63, 793-807.
18. Glenner, G.G. & Wong, C.W. (1984) Alzheimer's disease, initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun., 120, 885-890.
19. Goodman, Y. & Mattson, M.P. (1994) Secreted forms of beta-amyloid precursor protein protect hippocampal neurons against amyloid beta-peptide-induced oxidative injury. Exp. Neurol., 128, 1-12.
20. Grant, S.M., Morinville, A., Maysinger, D., Szyf, M. & Cuello, A.C. (1999) Phosphorylation of mitogen-activated protein kinase is altered in neuroectodermal cells overexpressing the human amyloid precursor protein 751 isoform. Brain Res. Mol Brain Res., 72, 115-120.
21. Grewal, S.S., York, R.D. & Stork, P.J. (1999) Extracellular-signal-regulated kinase signalling in neurons. Curr. Opin. Neurobiol., 9, 544-553.
22. Harada, J. & Sugimoto, M. (1999) Activation of caspase-3 in beta-amyloid-induced apoptosis of cultured rat cortical neurons. Brain Res., 842, 311- 323.
23. Hensley, K., Carney, J.M., Mattson, M.P., Aksenova, M., Harris, M., Wu, J.F., Floyd, R.A. & Butterfield, D.A. (1994) A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide, relevance to Alzheimer disease. Proc. Natl Acad. Sci., 91, 3270- 3274.
24. Honig, L.S. & Rosenberg, R.N. (2000) Apoptosis and neurologic disease. Am. J. Med., 108, 317-330.
25. Huang, X., Atwood, C.S., Hartshorn, M.A., Multhaup, G., Goldstein, L.E., Scarpa, R.C., Cuajungco, M.P., Gray, D.N., Lim, J., Moir, R.D., Tanzi, R.E. & Bush, A.I. (1999) The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry, 38, 7609-7616.
26. Ischiropoulos, H., Gow, A., Thom, S.R., Kooy, N.W., Royall, J.A. & Crow, J.P. (1999) Detection of reactive nitrogen species using 2,7-dichloro-dihydrofluorescein and dihydrorhodamine 123. Meth. Enzymol., 301, 367-373.
27. Ivins, K.J., Ivins, J.K., Sharp, J.P. & Cotman, C.W. (1999) Multiple pathways of apoptosis in PC12 cells. CrmA inhibits apoptosis induced by beta-amyloid. J. Biol. Chem., 274, 2107-2112.
28. Jimenez, L.A., Zanella, C., Fung, H., Janssen, Y.M., Vacek, P., Charland, C., Goldberg, J. & Mossman, B.T. (1997) Role of extracellular signal-regulated protein kinases in apoptosis by asbestos and H2O2. Am. J. Physiol., 273, 1029-1035.
29. Kala, S.V., Hasinoff, B.B. & Richardson, J.S. (1996) Brain samples from Alzheimer's patients have elevated levels of loosely bound iron. Internat. J. Neurosci., 86, 263-269.
30. Kuperstein, F., Reiss, N., Koudinova, N.V. & Yavin, E. (2001) Biphasic modulation of protein kinase C and enhanced cell death by amyloid beta peptide and anoxia in neuronal cultures. J. Neurochem., 76, 758-767.
31. 1-40-dependent ERK activation and enhances cell toxicity in primary neuronal cultures. Neurosci. Lett., 55, S31.
32. Loo, D.T., Copani, A., Pike, C.J., Whittemore, E.R., Walencewicz, A.J. & Cotman, C.W. (1993) Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc. Natl Acad. Sci. USA, 90, 7951-7955.
33. Lovell, M.A., Robertson, J.D., Teesdale, W.J., Campbell, J.L. & Markesbery, W.R. (1998) Copper, iron and zinc in Alzheimer's disease senile plaques. J.Neurol. Sci., 158, 47-52.
34. Lynch, T., Cherny, R.A. & Bush, A.I. (2000) Oxidative processes in Alzheimer's disease, the role of abeta-metal interactions. Exp. Gerontol., 35, 445-451.
35. Mangelus, M., Kroyter, A., Galron, R. & Sokolovsky, M. (2001) Reactive oxygen species regulate signaling pathways induced by M1 muscarinic receptors in PC12M1 cells. J. Neurochem., 76, 1701-1711.
36. Marin, N., Romero, B., Bosch-Morell, F., Llansola, M., Felipo, V., Roma, J. & Romero, F.J. (2000) Beta-amyloid-induced activation of caspase-3 in primary cultures of rat neurons. Mech. Ageing Dev., 119, 63-67.
37. Markesbery, W.R. & Carney, J.M. (1999) Oxidative alterations in Alzheimer's disease. Brain Pathol., 9, 133-146.
38. Markesbery, W.R. & Lovell, M.A. (1998) Four-hydroxynonenal, a product of lipid peroxidation is increased in the brain in Alzheimer's disease. Neurobiol. Aging, 19, 33-36.
39. Masters, C.L., Simms, G., Weinman, N.A., Multhaup, G., McDonald, B.L. & Beyreuther, K. (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl Acad. Sci., 82, 4245-4249.
40. Mattson, M.P. (1997) Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol. Rev., 77, 1081-1132.
41. McDonald, D.R., Bamberger, M.E., Combs, C.K. & Landreth, G.E. (1998) Beta-Amyloid fibrils activate parallel mitogen-activated protein kinase pathways in microglia and THP1 monocytes. J. Neurosci., 18, 4451-4460.
42. McIntosh, L.J., Trush, M.A. & Troncoso, J.C. (1997) Increased susceptibility of Alzheimer's disease temporal cortex to oxygen free radical-mediated processes. Free Radic. Biol. Med., 23, 183-190.
43. Miranda, S., Opazo, C., Larrondo, L.F., Munoz, F.J., Ruiz, F., Leighton, F. & Inestrosa, N.C. (2000) The role of oxidative stress in the toxicity induced by amyloid beta-peptide in Alzheimer's disease. Prog. Neurobiol., 62, 633-648.
44. Nishida, M., Maruyama, Y., Tanaka, R., Kontani, K., Nagao, T. & Kurose, H.G. (2000) alpha (i) and G alpha (o) are target proteins of reactive oxygen species. Nature, 408, 492-495.
45. Nitsch, R.M., Blusztajn, J.K., Pittas, A.G., Slack, B.E., Grow-don, J.H. & Wurtman, R.J. (1992) Evidence for a membrane defect in Alzheimer disease brain. Proc. Natl. Acad. Sci. USA, 89, 1671-1675.
46. Olivieri, G., Baysang, G., Meier, F., Muller-Spahn, F., Stahelin, H.B., Brockhaus, M. & Brack, C. (2001) N-acetyl-L-cysteine protects SHSY5Y neuroblastoma cells from oxidative stress and cell cytotoxicity. effects on beta-amyloid secretion and tau phosphorylation. J. Neurochem., 76, 224- 233.
47. Perry, G., Roder, H., Nunomura, A., Takeda, A., Friedlich, A.L., Zhu, X., Raina, A.K., Holbrook, N., Siedlak, S.L., Harris, P.L. & Smith, M.A. (1999) Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. Neuroreport, 10, 2411-2415.
48. Pettigrew, J.W., Moossy, J., Withers, G., McKeag, D. & Pan-chalingam, K. (1988) 31P nuclear magnetic resonance study of the brain in Alzheimer's disease, J. Neuropathol. Exp. Neurol., 47, 235-248.
49. Pyo, H., Jou, I., Jung, S., Hong, S. & Joe, E.H. (1999) Mitogen-activated protein kinases activated by lipopolysaccharide and beta-amyloid in cultured rat microglia. Neuroreport, 9, 871-874.
50. Rapoport, M. & Ferreira, A. (2000) PD98059 prevents neurite degeneration induced by fibrillar beta-amyloid in mature hippocampal neurons. J. Neurochem., 274, 125-133.
51. Rottkamp, C.A., Raina, A.K., Zhu, X., Gaier, E., Bush, A.I., Atwood, C.S., Chevion, M., Perry, G. & Smith, M.A. (2001) Redox-active iron mediates amyloid-beta toxicity. Free Radic. Biol. Med., 30, 447-450.
52. Rubinfeld, H., Hanoch, T. & Seger, R. (1999) Identification of a cytoplasmic-retention sequence in ERK2. J. Biol. Chem., 274, 30349-30352.
53. Samet, J.M., Graves, L.M., Quay, J., Dailey, L.A., Devlin, R.B., Ghio, A.J., Wu, W., Bromberg, P.A. & Reed, W. (1998) Activation of MAPKs in human bronchial epithelial cells exposed to metals. Am. J. Physiol., 275, 551-558.
54. Santiard-Baron, D., Gosset, P., Nicole, A., Sinet, P.M., Christen, Y. & Ceballos-Picot, I. (1999) Identification of beta-amyloid-responsive genes by RNA differential display, early induction of a DNA damage-inducible gene, gadd45. Exp. Neurol., 158, 206-213.
55. Satoh, T., Nakatsuka, D., Watanabe, Y., Nagata, I., Kikuchi, H. & Namura, S. (2000) Neuroprotection by MAPK/ERK kinase inhibition with U0126 against oxidative stress in a mouse neuronal cell line and rat primary cultured cortical neurons. Neurosci. Lett., 288, 163-166.
56. Selkoe, D. (1994) Alzheimer's disease, a central role for amyloid. J. Neuropathol. Exp. Neurol., 53, 438-447.
57. Seo, S.R., Chong, S.A., Lee, S.I., Sung, J.Y., Ahn, Y.S., Chung, K.C. & Seo, J.T. (2001) Zn (2+) -induced ERK activation mediated by reactive oxygen species causes cell death in differentiated PC12 cells. J. Neurochem., 78, 600-610.
58. Seubert, P., Vigo-Pelfrey, C., Esch, F., Lee, M., Dovey, H., Davis, D., Sinha, S., Schlossmacher, M., Whaley, J. & Swindlehurst, C. (1992) Isolation and quantification of soluble Alzheimer's beta-peptide from biological fluids. Nature, 359, 325-327.
59. Shirakata, Y., Ishii, K., Yagita, H., Okumura, K., Taniguchi, M. & Takemori, T. (1999) Distinct subcellular localization and substrate specificity of extracellular signal-regulated kinase in B cells upon stimulation with IgM and CD40. J. Immunol., 163, 6589-6597.
60. Smith, M.A., Rottkamp, C.A., Nunomura, A., Raina, A.K. & Perry, G. (2000) Oxidative stress in Alzheimer's disease. Biochim. Biophys. Acta, 1502, 139- 144.
61. Smits, H.A., de Vos, N.M., Wat, J.W., van der Bruggen, T., Verhoef, J. & Nottet, H.S. (2001) Intracellular pathways involved in TNF-alpha and superoxide anion release by Ab (1-42) -stimulated primary human macrophages. J. Neuroimmunol., 115, 144-151.
62. Stanciu, M., Wang, Y., Kentor, R., Burke, N., Watkins, S., Kress, G., Reynolds, I., Klann, E., Angiolieri, M.R., Johnson, J.W. & DeFranco, D.B. (2000) Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J. Biol. Chem., 275, 12200-12206.
63. Subbarao, K.V., Richardson, J.S. & Ang, L.C. (1990) Autopsy samples of Alzheimer's cortex show increased peroxidation in vitro. J. Neurochem., 55, 342-345.
64. Svennerholm, L. & Gottfries, C.G. (1994) Membrane lipids, selectively diminished in Alzheimer brains, suggest synapse loss as a primary event in early onset (type I) and demyelination in late-onset form (type II). J. Neurochem., 62, 1039-1047.
65. Tabaton, M., Nunzi, M.G., Xue, R., Usiak, M., Autilio-Gambetti, L. & Gambetti, P. (1994) Soluble amyloid beta-protein is a marker of Alzheimer amyloid in brain but not in cerebrospinal fluid. Biochem. Biophys. Res. Comm., 200, 1598-1603.
66. Tjernberg, L.O., Naslund, J., Lindqvist, F., Johansson, J., Karlstrom, A.R., Thyberg, J., Terenius, L. & Nordstedt, C. (1996) Arrest of beta-amyloid fibril formation by a pentapeptide ligand. J. Biol. Chem., 271, 8545-8548.
67. Uetsuki, T., Takemoto, K., Nishimura, I., Okamoto, M., Niinobe, M., Momoi, T., Miura, M. & Yoshikawa, K. (1999) Activation of neuronal caspase-3 by intracellular accumulation of wild-type Alzheimer amyloid precursor protein. J. Neurosci., 19, 6955-6964.
68. Varadarajan, S., Yatin, S., Aksenova, M. & Butterfield, D.A. (2000) Alzheimer's amyloid beta-peptide-associated free radical oxidative stress and neurotoxicity. J. Struct. Biol., 130, 184-208.
69. Wang, C.N., Chi, C.W., Lin, Y.L., Chen, C.F. & Shiao, Y.J. (2001) The neuroprotective Effects of phytoestrogens on amyloid beta protein-induced toxicity are mediated by abrogating the activation of caspase cascade in rat cortical neurons. J. Biol. Chem., 276, 5287-5295.
70. York, R.D., Yao, H., Dillon, T., Ellig, C.L., Eckert, S.P., McCleskey, E.W. & Stork, P.J. (1998) Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature, 392, 622-626.