Lithium inhibits Aβ-induced stress in endoplasmic reticulum of rabbit hippocampus but does not prevent oxidative damage and tau phosphorylation

Journal of Neuroscience Research

Volumn 71, Issue 6, 2003, Pages 853-862

  Ghribi, Othman ^a   Herman, Mary M ^c   Savory, John ^a,b,d  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^d UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

Caspase 12; Caspase 3; Cytochrome c; GSK 3 ; NF B

Indexed keywords

AMYLOID BETA PROTEIN; CASPASE 3; CYTOCHROME C; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LITHIUM; MITOCHONDRIAL DNA; TAU PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); CASPASE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PEPTIDE FRAGMENT;

ADOLESCENT; ALZHEIMER DISEASE; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN MITOCHONDRION; BRAIN PROTECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFECT; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME RELEASE; FEMALE; HIPPOCAMPUS; NEUROTOXICITY; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RABBIT; ANIMAL; DRUG ANTAGONISM; ENZYMOLOGY; IMMUNOHISTOCHEMISTRY; METABOLISM; MITOCHONDRION; MOUSE; PATHOLOGY; PHOSPHORYLATION; WESTERN BLOTTING;

AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASES; ENDOPLASMIC RETICULUM; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LITHIUM; MICE; MITOCHONDRIA; NF-KAPPA B; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; RABBITS; TAU PROTEINS;

EID: 0037443604     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.10511     Document Type: Article

References (63)

1. Allen JW, Eldadah BA, Huang X, Knoblach SM, Faden FI. 2001. Multiple caspases are involved in beta-amyloid-induced neuronal apoptosis. J Neurosci Res 65:45-53.
2. Alvarez G, Munoz-Montano JR, Satrustegui J, Avila J, Bogonez E, Diaz-Nido J. 1999. Lithium protects cultured neurons against beta-amyloid-induced neurodegeneration. FEBS Lett 453:260-264.
3. Atzori C, Ghetti B, Piva R, Srinivasan AN, Zolo P, Delisle MB, Mirra SS, Migheli A. 2001. Activation of the JNK/p38 pathway occurs in diseases characterized by tau protein pathology and is related to tau phosphorylation but not to apoptosis. J Neuropathol Exp Neurol 60:1190-1197.
4. Bales KR, Du Y, Dodel RC, Yan GM, Hamilton-Byrd E, Paul SM. 1998. The NF-κB/Rel family of proteins mediates Aβ-induced neurotoxicity and glial activation. Brain Res Mol Brain Res 57:63-72.
5. Bijur GN, De Sarno P, Jope RS. 2000. Glycogen synthase kinase-3beta facilitates staurosporine-and heat shock-induced apoptosis: protection by lithium. J Biol Chem 275:7583-7590.
6. Bijur GN, Jope RS. 2001. Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3β. J Biol Chem 276:37436-37442.
7. Butterfield DA, Drake J, Pocernich C, Castegna A. 2001. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol Med 7:548-554.
8. Citron M, Westaway D, Xia W, Carlson G, Diehl T, Levesque G, Johnson-Wood K, Lee M, Seubert P, Davis A, Kholodenko D, Motter R, Sherrington R, Perry B, Yao H, Strome R, Lieberburg I, Rommens J, Kim S, Schenk D, Fraser P, St. George HP, Selkoe DJ. 1997. Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat Med 3:67-72.
9. Duff K, Eckman C, Zehr C, Yu X, Prada CM, Perez-Tur J, Hutton M, Buee L, Harigaya Y, Yager D, Morgan D, Gordon MN, Holcomb L, Refolo L, Zenk B, Hardy J, Younkin S. 1996. Increased amyloid-β42(43) in brains of mice expressing mutant presenilin 1. Nature 383:710-713.
10. Ekinci FJ, Linsley MD, Shea TB. 2000. Beta-amyloid-induced calcium influx induces apoptosis in culture by oxidative stress rather than tau phosphorylation. Brain Res Mol Brain Res 76:389-395.
11. Ekinci FJ, Malik KU, Shea TB. 1999. Activation of the L voltage-sensitive calcium channel by mitogen-activated protein (MAP) kinase following exposure of neuronal cells to beta-amyloid. MAP kinase mediates beta-amyloid-induced neurodegeneration. J Biol Chem 274:30322-30327.
12. Gabbita SP, Lovell MA, Markesbery WR. 1998. Increased nuclear DNA oxidation in the brain in Alzheimer's disease. J Neurochem 71:2034-2040.
13. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F. 1995. Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373:523-527.
14. Gau JT, Steinhilb ML, Kao TC, D'Amato CJ, Gaut JR, Frey KA, Turner RS. 2002. Stable beta-secretase activity and presynaptic cholinergic markers during progressive central nervous system amyloidogenesis in Tg2576 mice. Am J Pathol 160:731-738.
15. Geula C, Wu C-K, Saroff D, Lorenzo A, Yuan M, Yankner BA. 1998. Aging renders the brain vulnerable to amyloid β-protein neurotoxicity. Nat Med 4:827-831.
16. Ghribi O, Herman MM, DeWitt DA, Forbes MS, Savory J. 2001a. A-β (1-42) and aluminum induce stress in the endoplasmic reticulum in rabbit hippocampus, involving nuclear translocation of gadd 153 and NF-κB. Brain Res Mol Brain Res 96:30-38.
17. Ghribi O, Herman MM, Forbes MS, DeWitt DA, Savory J. 2001b. GDNF protects against aluminum-induced apoptosis in rabbits by upregulating Bcl-2 and Bcl-XL and inhibiting mitochondrial Bax translocation. Neurobiol Dis 8:764-773.
18. Ghribi O, Herman MM, Savory J. 2002a. The endoplasmic reticulum is the main site for caspase-3 activation following aluminum-induced neurotoxicity in rabbit hippocampus. Neurosci Lett 324:217-221.
19. Ghribi O, Herman MM, Spaulding NK, Savory J. 2002b. Lithium inhibits aluminum-induced apoptosis in rabbit hippocampus, by preventing cytochrome c translocation, Bcl-2 decrease, Bax elevation and caspase-3 activation. J Neurochem 82:137-145.
20. Gotz J, Chen F, van Dorpe J, Nitsch RM. 2001. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Aβ 42 fibrils. Science 293:1491-1495.
21. Graur D, Duret L, Gouy M. 1996. Phylogenetic position of the order Lagomorpha (rabbits, hares and allies). Nature 379:333-335.
22. Grimes CA, Jope RS. 2001. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 65:391-426.
23. Guerrini L, Blasi F, Denis-Donini S. 1995. Synaptic activation of NF-kappa B by glutamate in cerebellar granule neurons in vitro. Proc Natl Acad Sci USA 92:9077-9081.
24. Hartigan JA, Johnson GV. 1999. Transient increases in intracellular calcium result in prolonged site-selective increases in Tau phosphorylation through a glycogen synthase kinase 3beta-dependent pathway. J Biol Chem 274:21395-21401.
25. Henshall DC, Chen J, Simon RP. 2000. Involvement of caspase-3-like protease in the mechanism of cell death following focally evoked limbic seizures. J Neurochem 74:1215-1223.
26. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, Woodgett JR. 2000. Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406:86-90.
27. Iida T, Furuta A, Nishioka K, Nakabeppu Y, Iwaki T. 2002. Expression of 8-oxoguanine DNA glycosylase is reduced and associated with neurofibrillary tangles in Alzheimer's disease brain. Acta Neuropathol (Berl) 103:20-25.
28. Javelaud D, Besancon F. 2001. NF-κB activation results in rapid inactivation of JNK in TNF α-treated Ewing sarcoma cells: a mechanism for the anti-apoptotic effect of NF-κB. Oncogene 20:4365-4372.
29. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C. 1997. Transcription factor NF-κB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc Natl Acad Sci USA 94:2642-2647.
30. Kaltschmidt, B, Uherek M, Wellmann H, Volk B, Kaltschmidt C. 1999. Inhibition of NF-κB potentiates amyloid beta-mediated neuronal apoptosis. Proc Natl Acad Sci USA 96:9409-9414.
31. King, TD, Bijur GN, Jope RS. 2001. Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3β and attenuated by lithium. Brain Res 919:106-114.
32. Klein PS, Melton DA. 1996. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93:8455-8459.
33. Lesort M, Jope RS, Johnson GV. 1999. Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3β and Fyn tyrosine kinase. J Neurochem 72:576-584.
34. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, Yen SH, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton M, McGowan E. 2001. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293:1487-1491.
35. Loberg RD, Vesely E, Brosius FC III. 2002. Enhanced glycogen synthase kinase-3β activity mediates hypoxia-induced apoptosis of vascular smooth muscle cells and is prevented by glucose transport and metabolism. J Biol Chem 277:41667-41673.
36. Lovell MA, Gabbita SP, Markesbery WR. 1999. Increased DNA oxidation and decreased levels of repair products in Alzheimer's disease ventricular CSF. J Neurochem 72:771-776.
37. Lovell MA, Xie C, Markesbery WR. 2000. Decreased base excision repair and increased helicase activity in Alzheimer's disease brain. Brain Res 855:116-123.
38. Markesbery WR, Carney JM. 1999. Oxidative alterations in Alzheimer's disease. Brain Pathol 9:133-146.
39. Mattson MP, Chan SL. 2001. Dysregulation of cellular calcium homeostasis in Alzheimer's disease: bad genes and bad habits. J Mol Neurosci 17:205-224.
40. Mattson MP, Culmsee C, Yu Z, Camandola S. 2000. Roles of nuclear factor κB in neuronal survival and plasticity. J Neurochem 74:443-456.
41. Mattson MP, Gary DS, Chan SL, Duan W. 2001. Perturbed endoplasmic reticulum function, synaptic apoptosis and the pathogenesis of Alzheimer's disease. Biochem Soc Symp 67:151-162.
42. McKee AC, Kowall NW, Schumacher JS, Beal MF. 1998. The neurotoxicity of amyloid β protein in aged primates. Amyloid 5:1-9.
43. Mecocci P, MacGarvey U, Beal MF. 1994. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann Neurol 36:747-751.
44. Moyer TP 1999. Therapeutic drug monitoring. In: Burtis CA, Ashwood ER, editors. Tietz textbook of clinical chemistry. Philadelphia: PAWB Saunders Company. p 892.
45. Mudher A, Lovestone S. 2002. Alzheimer's disease-do tauists and baptists finally shake hands? Trends Neurosci 25:22-26.
46. Munoz-Montano JR, Moreno FJ, Avila J, Diaz-Nido J. 1997. Lithium inhibits Alzheimer's disease-like tau protein phosphorylation in neurons. FEBS Lett 411:183-188.
47. Nakagawa T, Yuan J. 2000. Cross-talk between two cysteine protease families: activation of caspase-12 by calpain in apoptosis. J Cell Biol 150:887-894.
48. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 403:98-103.
49. Pahl HL, Baeuerle PA. 1995. A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by transcription factor NF-κB. EMBO J 14:2580-2588.
50. Pahl HL, Sester M, Burgert HG, Baeuerle PA. 1996. Activation of transcription factor NF-κB by the adenovirus E3/19K protein requires its ER retention. J Cell Biol 132:511-522.
51. Plyte SE, Hughes K, Nikolakaki E, Pulverer BJ, Woodgett JR. 1992. Glycogen-synthase kinase-3 - functions in oncogenesis and development. Biochim Biophys Acta 1114:147-162.
52. Reynolds CH, Betts JC, Blackstock WP, Nebreda AR, Anderton BH. 2000. Phosphorylation sites on tau identified by nanoelectrospray mass spectrometry: differences in vitro between the mitogen-activated protein kinases ERK2, c-Jun N-terminal kinase and P38, and glycogen synthase kinase-3β. J Neurochem 74:1587-1595.
53. Reynolds CH, Utton MA, Gibb GM, Yates A, Anderton BH. 1997. Stress-activated protein kinase/c-jun N-terminal kinase phosphorylates tau protein. J Neurochem 68:1736-1744.
54. Saez-Valero J, Angeretti N, Forloni G. 2000. Caspase-3 activation by beta-amyloid and prion protein peptides is independent from their neurotoxic effect. Neurosci Lett 293:207-210.
55. Sanchez C, Perez M, Avila J. 2000. GSK3β-mediated phosphorylation of the microtubule-associated protein 2C (MAP2C) prevents microtubule bundling. Eur J Cell Biol 79:252-260.
56. Selznick LA, Zheng TS, Flavell RA, Rakic P, Roth KA. 2000. Amyloid beta-induced neuronal death is bax-dependent but caspase-independent. J Neuropathol Exp Neurol 59:271-279.
57. Smith MA, Rottkamp CA, Nunomura A, Raina AK, Perry G. 2000. Oxidative stress in Alzheimer's disease. Biochim Biophys Acta 1502:139-144.
58. Takashima A, Honda T, Yasutake K, Michel G, Murayama O, Murayama M, Ishiguro K, Yamaguchi H. 1998. Activation of tau protein kinase I/glycogen synthase kinase-3β by amyloid beta peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci Res 31:317-323.
59. Takashima A, Noguchi K, Sato K, Hoshino T, Imahori K. 1993. Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. Proc Natl Acad Sci USA 90:7789-7793.
60. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, Lin A. 2001. Inhibition of JNK activation through NF-κB target genes. Nature 414:313-317.
61. Troy CM, Rabacchi SA, Xu Z, Maroney AC, Connors TJ, Shelanski ML, Greene LA. 2001. β-Amyloid-induced neuronal apoptosis requires c-Jun N-terminal kinase activation. J Neurochem 77:157-164.
62. Wang QM, Fiol CJ, DePaoli-Roach AA, Roach PJ. 1994. Glycogen synthase kinase-3β is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J Biol Chem 269:14566-14574.
63. Woodruff-Pak DS, Trojanowski JQ. 1996. The older rabbit as an animal model: implications for Alzheimer's disease. Neurobiol Aging 17:283-290.