Protracted lithium treatment protects against the ER stress elicited by thapsigargin in rat PC12 cells: Roles of intracellular calcium, GRP78 and Bcl-2

Pharmacogenomics Journal

Volumn 5, Issue 2, 2005, Pages 102-111

  Hiroi, T ^a   Wei, H ^a   Hough, C ^b   Leeds, P ^a   Chuang, D M ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Cytoprotection; ER stress; GRP78; Lithium; PC12 cells; Thapsigargin

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CALCIUM ION; CURCUMIN; GLUCOSE REGULATED PROTEIN 78; LACTATE DEHYDROGENASE; LITHIUM; MOOD STABILIZER; PROTEIN BCL 2; PROTEIN C FOS; THAPSIGARGIN; TRANSCRIPTION FACTOR AP 1; VALPROIC ACID;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DEATH; CELL PROTECTION; CELL STRAIN; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; DOWN REGULATION; DRUG MECHANISM; ENDOPLASMIC RETICULUM; ENZYME ASSAY; GEL MOBILITY SHIFT ASSAY; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CALCIUM; CALCIUM-TRANSPORTING ATPASES; CELL SURVIVAL; CURCUMIN; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; HEAT-SHOCK PROTEINS; LITHIUM; MOLECULAR CHAPERONES; NEUROPROTECTIVE AGENTS; PC12 CELLS; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-FOS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THAPSIGARGIN; TRANSCRIPTION FACTOR AP-1; VALPROIC ACID;

EID: 16344382201     PISSN: 1470269X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.tpj.6500296     Document Type: Article

References (69)

1. Rao RV, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Different 2004; 11: 372-380.
2. Ma Y, Hendershot LM. The mammalian endoplasmic reticulum as a sensor for cellular stress. Cell Stress Chaperones 2002; 7: 222-229.
3. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 2004; 14: 20-28.
4. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403: 98-103.
5. 2+ disturbances, and cell death in renal epithelial cells. J Biol Chem 1997; 272: 21751-21759.
6. Wei MC, Zong WX, Cheng EHY, Lindsten T, Panoutsakopoulou V, Ross AJ et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730.
7. Germain M, Mathai JP, Shore GC. BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J Biol Chem 2002; 277: 18053-18060.
8. Mattson MP, LaFerla FM, Chan SL, Leissring MA, Shepel PN, Geiger JD. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci 2000; 23: 222-229.
9. Sherman MY, Goldberg AL. Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 2001; 29: 15-32.
10. Paschen W. Endoplasmic reticulum: a primary target in various acute disorders and degenerative diseases of the brain. Cell Calcium 2003; 34: 365-383.
11. Nonaka S, Hough C, Chuang D-M. Chronic lithium treatment robustly protects CNS neurons against excitotoxicity by inhibiting NMDA receptor-mediated calcium influx. Proc Natl Acad Sci USA 1998; 95: 2642-2647.
12. Hashimoto R, Hough C, Nakazawa T, Yamamoto T, Chuang D-M. Lithium protection against glutamate excitotoxicity in rat cerebral cortical neurons: involvement of NMDA receptor inhibition possibly by decreasing NR2B tyrosine phosphorylation. J Neurochem 2002; 80 589-597.
13. Wei H, Leeds PR, Qian Y, Wei W, Chen R-W, Chuang D-M. β-Amyloid-induced death of PC 12 cells and cerebellar neurons is inhibited by long-term lithium treatment. Eur J Pharmacol 2000; 392: 117-123.
14. Bijur GN, De Sarno P, Jope RS. Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J Biol Chem 2000; 275: 7583-7590.
15. Kanai H, Sawa A, Chen R-W, Leeds P, Chuang D-M. Valproic acid inhibits histone deacetylase activity and suppresses excitotoxicity-induced GAPDH nuclear accumulation and apoptotic death in neurons. Pharmacogenomics J 2004; 4: 336-344.
16. Nonaka S, Katsube N, Chuang D-M. Lithium protects rat cerebellar granule cells against apoptosis induced by anticonvulsants, phenytoin and carbamazepine. J Pharmacol Exp Ther 1998; 286: 539-547.
17. Li R, Shen Y, El-Mallakh RS. Lithium protects against ouabain-induced cell death. Lithium 1994; 5: 211-216.
18. Hennion JP, El-Masri MA, Huff MO, El-Mallakh RS. Evaluation of neuroprotection by lithium and valproic acid against ouabain-induced cell damage. Bipolar Disord 2002; 4: 201-206.
19. D'Mello SR, Anelli R, Calissano P. Lithium induces apoptosis in immature cerebellar granule cells but promotes survival of mature neurons. Exp Cell Res 1994; 211: 332-338.
20. Alvarez G, Munoz-Montano JR, Satrustegui J, Avila J, Bogonez E, Diaz-Nido J. Lithium protects cultured neurons against beta-amyloid-induced neurodegeneration. FEBS Lett 1999; 453: 260-264.
21. Tseng WP, Lin-Shiau SY. Long-term lithium treatment prevents neurotoxic effects of beta-bungarotoxin in primary cultured neurons. J Neurosci Res 2002; 69: 633-641.
22. Nonaka S, Chuang D-M. Neuroprotective effects of chronic lithium on focal cerebral ischemia in rats. Neuroreport 1998; 9 2081-2084.
23. Ren M, Senatorov VV, Chen R-W, Chuang D-M. Post-insult treatment with lithium reduces brain damage and facilitates neurological recovery in a rat ischemia/reperfusion model. Proc Natl Acad Sci USA 2003; 100: 6210-6215.
24. Xu JH, Culman J, Blume A, Brecht S, Gohlke P. Chronic treatment with a low dose of lithium protects the brain against ischemic injury by reducing apoptotic death. Stroke 2003; 34: 1287-1292.
25. Wei H, Qin ZH, Senatorov VV, Wei W, Wang Y, Qian Y et al. Lithium suppresses excitotoxicity-induced striatal lesions in a rat model of Huntington's disease. Neuroscience 2001; 106: 603-612.
26. Senatorov VV, Ren M, Kanai H, Wei H, Chuang D-M. Short-term lithium treatment promotes neuronal survival and proliferation in rat striatum infused with quinolinic acid, an excitotoxic model of Huntington's disease. Mol Psychiatry 2004; 9: 371-385.
27. Pascual T, Gonzalez JL. A protective effect of lithium on rat behaviour altered by ibotenic acid lesions of the basal forebrain cholinergic system. Brain Res 1995; 695: 289-292.
28. Sparapani M, Virgili M, Ortali F, Contestabile A. Effects of chronic lithium treatment on ornithine decarboxylase induction and excitotoxic neuropathology in the rat. Brain Res 1997; 765: 164-168.
29. Hashimoto R, Takei N, Shimazu K, Christ L, Lu B, Chuang D-M. Lithium induces brain-derived neurotrophic factor and activates TrkB in rodent cortical neurons: an essential step for neuroprotection against glutamate excitotoxicity. Neuropharmacology 2002; 43: 1173-1179.
30. Chalecka-Franaszek E, Chuang D-M. Lithium activates the serine/ threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc Natl Acad Sci USA 1999; 96: 8745-8750.
31. Kopnisky KL, Chalecka-Franaszek E, Gonzalez-Zulueta M, Chuang D-M. Chronic lithium treatment antogonizes glutamine-induced decrease of phosphorylated CREB in neurons by reducing PP1 and increasing MEK activities. Neurosci 2003; 116: 425-435.
32. Einat H, Yuan PX, Gould TD, Li JL, Du JH, Zhang L et al. The role of the extracellular signal-regulated kinase signaling pathway in mood modulation. J Neurosci 2003; 23: 7311-7316.
33. Klein PS, Melton DA. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 1996; 93: 8455-8459.
34. De Sarno P, Li X, Jope RS. Regulation of Akt and glycogen synthase kinase-3β phosphorylation by sodium valproate and lithium. Neuropharmacology 2002; 43: 1158-1164.
35. Zhang F, Phiel CJ, Spece L, Gurvich N, Klein PS. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium: evidence for autoregulation of GSK-3. J Biol Chem 2003; 278: 33067-33077.
36. Hashimoto R, Fujimaki K, Jeong MR, Christ L, Chuang D-M. Lithium-induced inhibition of Src tyrosine kinase in rat cerebral cortical neurons: a role in neuroprotection against N methyl-D-aspartate receptor-mediated excitotoxicity. FEBS Lett 2003; 538: 145-148.
37. Song L, De Sarno P, Jope RS. Central role of glycogen synthase kinase-3β in endoplasmic reticulum stress-induced caspase-3 activation. J Biol Chem 2002; 277: 44701-44708.
38. Thastrup O, Cullen PJ, Drobak BK, Hanley MR, Dawson AP. Thapsigargin, a tumor promoter, discharges intracellular Ca-2+ stores by specific-inhibition of the endoplasmic-reticulum Ca-2+-ATPase. Proc Natl Acad Sci USA 1990; 87: 2466-2470.
39. Katayama T, Imaizumi K, Sato N, Miyoshi K, Kudo T, Hitomi J et al. Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response. Nat Cell Biol 1999; 1: 479-485.
40. Yu Z, Luo H, Fu W, Mattson MP. The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: suppression of oxidative stress and stabilization of calcium homeostasis. Exp Neurol 1999; 155: 302-314.
41. Aoki T, Koike T, Nakano T, Shibahara K, Kondo S, Kikuchi H et al. Induction of Bip mRNA upon programmed cell death of differentiated PC12 cells as well as rat sympathetic neurons. J Biochem (Tokyo) 1997; 121: 122-127.
42. He H, McColl K, Distelhorst CW. Involvement of c-Fos in signaling grp78 induction following ER calcium release. Oncogene 2000; 19: 5936-5943.
43. Kalasapudi VD, Sheftel G, Divish MM, Papolos DF, Lachman HM. Lithium augments fos protoonocogene expression in PC12 phoechromocytoma cells: implications for therapeutic action of lithium. Brain Res 1990; 521: 47-54.
44. 3-muscarinic acetylcholine receptors in cultured cerebellar granule cells. Neurochem Int 1993; 22: 395-403.
45. Sikora E, Bielak-Zmijewska A, Piwocka K, Skierski J, Radziszewska E. Inhibition of proliferation and apoptosis of human and rat T lymphocytes by curcumin, a curry pigment. Biochem Pharmacol 1997; 54: 899-907.
46. 2+ fluxes. Proc Natl Acad Sci USA 1994; 91: 6569-6573.
47. He H, Lam M, McCormick TS, Distelhorst CW. Maintenance of calcium homeostasis in the endoplasmic reticulum by Bcl-2. J Cell Biol 1997; 138: 1219-1228.
48. Chen R-W, Chuang D-M. Long term lithium treatment suppresses p53 and Bax expression but increases Bcl-2 expression. A prominent role in neuroprotection against excitotoxicity. J Biol Chem 1999; 274 6039-6042.
49. Chen G, Zeng WZ, Yuan PX, Huang LD, Jiang YM, Zhao ZH et al. The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J Neurochem 1999; 72: 879-882.
50. Wang JF, Bown C, Young LT. Differential display PCR reveals novel targets for the mood-stabilizing drug valproate including the molecular chaperone GRP78. Mol Pharmacol 1999; 55: 521-527.
51. Wei H, Wei W, Bredesen DE, Perry DC. Bcl-2 protects against apoptosis in neuronal cell line caused by thapsigargin-induced depletion of intracellular calcium stores. J Neurochem 1998; 70: 2305-2314.
52. Wei H, Perry DC. Dantrolene is cytoprotective in two models of neuronal cell death. J Neurochem 1996; 67: 2390-2398.
53. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999; 13: 1211-1233.
54. Miyake H, Hara I, Arakawa S, Kamidono S. Stress protein GRP78 prevents apoptosis induced by calcium ionophore, ionomycin, but not by glycosylation inhibitor, tunicamycin, in human prostate cancer cells. J Cell Biochem 2000; 77: 396-408.
55. Rao RV, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T et al. Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett 2002; 514: 122-128.
56. Ghribi O, Herman MM, Savory J. Lithium inhibits Aβ-induced stress in endoplasmic reticulum of rabbit hippocampus but does not prevent oxidative damage and tau phosphorylation. J Neurosci Res 2003; 71: 853-862.
57. Ozaki N, Chuang D-M. Lithium increases transcription factor binding to AP-1 and cyclic AMP-responsive element in cultured neurons and rat brain. J Neurochem 1997; 69: 2336-2344.
58. 2-terminal kinases in vitro and in the CNS in vivo. J Neurochem 1999; 73: 2299-2309.
59. Chen RW, Qin ZH, Ren M, Kanai H, Chalecka-Franaszek E, Leeds P et al. Regulation of c-Jun N-terminal kinase, p38 kinase and AP-1 DNA binding in cultured brain neurons: roles in glutamate excitotoxicity and lithium neuroprotection. J Neurochem 2003; 84: 566-575.
60. Karin M. Mitogen-activated protein kinase cascades as regulators of stress responses. Ann NY Acad Sci 1998; 851: 139-146.
61. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004; 305: 626-629.
62. Bown CD, Wang JF, Young LT. Increased expression of endoplasmic reticulum stress proteins following chronic valproate treatment of rat C6 glioma cells. Neuropharmacology 2000; 39: 2162-2169.
63. Chen B, Wang JF, Young LT. Chronic valproate treatment increases expression of endoplasmic reticulum stress proteins in the rat cerebral cortex and hippocampus. Biol Psychiatry 2000; 48: 658-664.
64. Chen G, Yuan P, Hawver DB, Potter WZ, Manji HK. Increase in AP-1 transcription factor DNA binding activity by valproic acid. Neuropsychopharm 1997; 16: 238-245.
65. Gould TD, Quiroz JA, Singh J, Zarate CA, Manji HK. Emerging experimental therapeutics for bipolar disorder: insights from the molecular and cellular actions of current mood stabilizers. Mol Psychiatry 2004; 9: 734-755.
66. Drevets WC. Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders. Curr Opin Neurobiol 2001; 11: 240-249.
67. Liu Y, Peterson DA, Kimura H, Schubert D. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2, 5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 1997; 69: 581-593.
68. Hough CJ, Irwin RP, Gao XM, Rogawski MA, Chuang D-M. Carbamazepine inhibition of N-methyl-D-aspartate-evoked calcium influx in rat cerebellar granule cells. J Pharmacol Exp Ther 1996; 276: 143-149.
69. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985; 260: 3440-3450.