Bip Enhanced the Association of GSK-3β with Tau during ER Stress Both in vivo and in vitro

Journal of Alzheimer's Disease

Volumn 29, Issue 4, 2012, Pages 727-740

  Liu, Zan Chao ^a   Fu, Zheng Qi ^a,b   Song, Jie ^a   Zhang, Jia Yu ^a   Wei, Yu Ping ^a   Chu, Jiang ^a   Han, Li ^a   Qu, Na ^a   Wang, Jian Zhi ^a   Tian, Qing ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b JIANGHAN UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Bip; endoplasmic reticulum stress; GSK 3 ; tau

Indexed keywords

BETA CATENIN; GLUCOSE REGULATED PROTEIN 78; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; PROTEIN KINASE FYN; PROTEIN TYROSINE PHOSPHATASE 1B; SMALL INTERFERING RNA; TAU PROTEIN; TUNICAMYCIN;

ANIMAL EXPERIMENT; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT;

EID: 84860163968     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-111898     Document Type: Article

References (58)

1. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM (1986) Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 261, 6084-6089. (Pubitemid 17207447)
2. Huang HC, Jiang ZF (2009) Accumulated amyloid-beta peptide and hyperphosphorylated tau protein: Relationship and links in Alzheimer's disease. J Alzheimers Dis 16, 15-27.
3. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83, 4913-4917.
4. Hernandez F, Avila J (2008) Tau aggregates and tau pathology. J Alzheimers Dis 14, 449-452.
5. Shipton OA, Leitz JR, Dworzak J, Acton CE, Tunbridge EM, Denk F, Dawson HN, Vitek MP, Wade-Martins R, Paulsen O, Vargas-Caballero M (2011) Tau protein is required for amyloid fj-induced impairment of hippocampal long-term potentiation. J Neurosci 31, 1688-1692.
6. Morris M, Maeda S, Vossel K, Mucke L (2011) The many faces of tau. Neuron 70, 410-426.
7. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: Disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7, 1013-1030.
8. Kapoor A, Sanyal AJ (2009) Endoplasmic reticulum stress and the unfolded protein response. Clin Liver Dis 13, 581-590.
9. Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: Cell life and death decisions. J Clin Invest 115, 2656-2664. (Pubitemid 41434389)
10. Lindholm D, Wootz H, Korhonen L (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13, 385-392.
11. Katayama T, Imaizumi K, Manabe T, Hitomi J, Kudo T, Tohyama M (2004) Induction of neuronal death by ER stress in Alzheimer's disease. J Chem Neuroanat 28, 67-78. (Pubitemid 39198955)
12. Matus S, Glimcher LH, Hetz C (2011) Protein folding stress in neurodegenerative diseases: A glimpse into the ER. Curr Opin Cell Biol 23, 239-252.
13. Hoozemans JJ, Veerhuis R, Van Haastert ES, Rozemuller JM, Baas F, Eikelenboom P, Scheper W (2005) The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol 110, 165-172. (Pubitemid 41245205)
14. Hoozemans JJ, Van Haastert ES, Nijholt DA, Rozemuller AJ, Eikelenboom P, Scheper W (2009) The unfolded protein response is activated in pretangle neurons in Alzheimer's disease hippocampus. Am J Pathol 174, 1241-1251.
15. Ling ZQ, Tian Q, Wang L, Fu ZQ, Wang XC, Wang Q, Wang JZ (2009) Constant illumination induces Alzheimerlike damages with endoplasmic reticulum involvement and the protection of melatonin. J Alzheimers Dis 16, 287-300.
16. Ishiguro K, Shiratsuchi A, Sato S, Omori A, Arioka M, Kobayashi S, Uchida T, Imahori K (1993) Glycogen synthase kinase 3 beta is identical to tau protein kinase I generating several epitopes of paired helical filaments. FEBS Lett 325, 167-172. (Pubitemid 23186470)
17. Pei JJ, Braak E, Braak H, Grundke-Iqbal I, Iqbal K, Winblad B, Cowburn RF (1999) Distribution of active glycogen synthase kinase 3beta in brains staged for Alzheimer disease neurofibrillary changes. J Neuropathol Exp Neurol 58, 1010-1019. (Pubitemid 29441929)
18. Wang Y, Zhang JX, Du XX, Zhao L, Tian Q, Zhu LQ, Wang SH, Wang JZ (2008) Temporal correlation of the memory deficit with Alzheimer-like lesions induced by activation of glycogen synthase kinase-3. J Neurochem 106, 2364-2374.
19. Zhu LQ, Wang SH, Liu D, Yin YY, Tian Q, Wang XC, Wang Q, Chen JG, Wang JZ (2007) Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments. J Neurosci 27, 12211-12220. (Pubitemid 350085482)
20. Salminen A, Kauppinen A, Suuronen T, Kaarniranta K, Ojala J (2009) ER stress in Alzheimer's disease: A novel neuronal trigger for inflammation and Alzheimer's pathology. J Neu-roinflammation 6, 41.
21. Song L, De Sarno P, Jope RS (2002) Central role of glycogen synthase kinase-3beta in endoplasmic reticulum stress-induced caspase-3 activation. J Biol Chem 277, 44701-44708. (Pubitemid 36159060)
22. Kim AJ, Shi Y, Austin RC, Werstuck GH (2005) Valproate protects cells from ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3. J Cell Sci 118, 89-99. (Pubitemid 40277107)
23. Fu ZQ, Yang Y, Song J, Jiang Q, Liu ZC, Wang Q, Zhu LQ, Wang JZ, Tian Q (2010) LiCl attenuates thapsigargin-Induced tau hyperphosphorylation by inhibiting GSK-3 fj in vivo and in vitro. J Alzheimers Dis 21, 1107-1117.
24. Qian Y, Zheng Y, Ramos KS, Tiffany-Castiglioni E (2005) GRP78 compartmentalized redistribution in Pb-treated glia: Role of GRP78 in lead-induced oxidative stress. Neurotoxi-cology 26, 267-275. (Pubitemid 40248444)
25. Chiou JF, Tai CJ, Huang MT, Wei PL, Wang YH, An J, Wu CH, Liu TZ, Chang YJ (2010) Glucose-regulated protein 78 is a novel contributor to acquisition of resistance to sorafenib in hepatocellular carcinoma. Ann Surg Oncol 17, 603-612.
26. Li HL, Wang HH, Liu SJ, Deng YQ, Zhang YJ, Tian Q, Wang XC, Chen XQ, Yang Y, Zhang JY, Wang Q, Xu H, Liao FF, Wang JZ (2007) Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc Natl Acad Sci USA 104, 3591-3596. (Pubitemid 46364203)
27. Liu XA, Liao K, Liu R, Wang HH, Zhang Y, Zhang Q, Wang Q, Li HL, Tian Q, Wang JZ (2010) Tau dephosphorylation potentiates apoptosis with the mechanisms involving a failed dephosphorylation/activation of Bcl-2. J Alzheimers Dis 19, 953-962.
28. Zhang YJ, Xu YF, Liu YH, Yin J, Li HL, Wang Q, Wang JZ (2006) Peroxynitrite induces Alzheimer-like tau modifications and accumulation in rat brain and its underlying mechanisms. FASEB J 20, 1431-1442. (Pubitemid 44943851)
29. Liu SJ, Zhang JY, Li HL, Fang ZY, Wang Q, Deng HM, Gong CX, Grundke-Iqbal I, Iqbal K, Wang JZ (2004) Tau becomes a more favorable substrate for GSK-3 when it is prephosphorylated by PKA in rat brain. J Biol Chem 279, 50078-50088. (Pubitemid 39577819)
30. Tian Q, Zhang JX, Zhang Y, Wu F, Tang Q, Wang C, Shi ZY, Zhang JH, Liu S, Wang Y, Zhang Q, Wang JZ (2009) Bipha-sic effects of forskolin on tau phosphorylation and spatial memory in rats. J Alzheimers Dis 17, 631-642.
31. Zhang CE, Tian Q, Wei W, Peng JH, Liu GP, Zhou XW, Wang Q, Wang DW, Wang JZ (2008) Homocysteine induces tau phosphorylation by inactivating protein phosphatase 2A in rat hippocampus. Neurobiol Aging 29, 1654-1665.
32. Wang JZ, Liu F (2008) Microtubule-associated protein tau in development, degeneration and protection of neurons. Prog Neurobiol 85, 148-175.
33. Liu XA, Zhu LQ, Zhang Q, Shi HR, Wang SH, Wang Q, Wang JZ (2008) Estradiol attenuates tau hyperphosphoryla-tion induced by upregulation of protein kinase-A. Neurochem Res 33, 1811-1820.
34. Wang JZ, Grundke-Iqbal I, Iqbal K (2007) Kinases and phos-phatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur J Neurosci 25, 59-68. (Pubitemid 46098893)
35. Liu R, Wang JZ (2009) Protein phosphatase2Ain Alzheimer's disease. Pathophysiology 16, 273-277.
36. Pei JJ, Tanaka T, Tung YC, Braak E, Iqbal K, Grundke-Iqbal I (1997) Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J Neuropathol Exp Neurol 56, 70-78. (Pubitemid 127470328)
37. Liu SJ, Zhang AH, Li HL, Wang Q, Deng HM, Netzer WJ, Xu H, Wang JZ (2003) Overactivation of glycogen synthase kinase-3byinhibitionofphosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of tau and impairment of spatial memory. J Neurochem 87, 1333-1344. (Pubitemid 38020568)
38. Zhu LQ, Liu D, Hu J, Cheng J, Wang SH, Wang Q, Wang F, Chen JG, Wang JZ (2010) GSK-3 beta inhibits presynap-tic vesicle exocytosis by phosphorylating P/Q-type calcium channel and interrupting SNARE complex formation. J Neu-rosci 30, 3624-3633.
39. Srivastava RK, Sollott SJ, Khan L, Hansford R, Lakatta EG, Longo DL (1999) Bcl-2 and Bcl-X (L) block thapsigargin-induced nitric oxide generation, c-Jun NH (2)-terminal kinase activity, and apoptosis. Mol Cell Biol 19, 5659-5674. (Pubitemid 29339923)
40. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666. (Pubitemid 30070916)
41. Goedert M, Hasegawa M, Jakes R, Lawler S, Cuenda A, Cohen P (1997) Phosphorylation of microtubule-associated protein tau by stress-activated protein kinases. FEBS Lett 409, 57-62. (Pubitemid 27248567)
42. Reynolds CH, Nebreda AR, Gibb GM, Utton MA, Ander-ton BH (1997) Reactivating kinase/p38 phosphorylates tau protein in vitro. J Neurochem 69, 191-198. (Pubitemid 27274172)
43. Reynolds CH, Betts JC, Blackstock WP, Nebreda AR, Ander-ton 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-3beta. J Neurochem 74, 1587-1595. (Pubitemid 30163980)
44. Kim I, Shu CW, Xu W, Shiau CW, Grant D, Vasile S, Cosford ND, Reed JC (2009) Chemical biology investigation of cell death pathways activatedby endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J Biol Chem 284, 1593-1603.
45. Hosoi T, Hyoda K, Okuma Y, Nomura Y, Ozawa K (2007) Akt up-and down-regulation in response to endoplasmic reticu-lum stress. Brain Res 1152, 27-31. (Pubitemid 46802507)
46. Griffin RJ, Moloney A, Kelliher M, Johnston JA, Ravid R, Dockery P, O'Connor R, O'Neill C (2005) Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J Neurochem 93, 105-117. (Pubitemid 40463520)
47. Pei JJ, Khatoon S, An WL, Nordlinder M, Tanaka T, Braak H, Tsujio I, Takeda M, Alafuzoff I, Winblad B, Cowburn RF, Grundke-Iqbal I, Iqbal K (2003) Role of protein kinase B in Alzheimer's neurofibrillary pathology. Acta Neuropathol 105, 381-392. (Pubitemid 36798832)
48. Lesort M, Jope RS, Johnson GV (1999) Insulin transiently increases tau phosphorylation: Involvement of glycogen syn-thase kinase-3beta and Fyn tyrosine kinase. J Neurochem 72, 576-584. (Pubitemid 29055219)
49. Grimes CA, Jope RS (2001) The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 65, 391-426. (Pubitemid 32781670)
50. Ho GJ, Hashimoto M, Adame A, Izu M, Alford MF, Thal LJ, Hansen LA, Masliah E (2005) Altered p59Fyn kinase expression accompanies disease progression in Alzheimer's disease: Implications for its functional role. Neurobiol Aging 26, 625-635. (Pubitemid 40228754)
51. Chin J, Palop JJ, Puoliväli J, Massaro C, Bien-Ly N, Gerstein H, Scearce-Levie K, Masliah E, Mucke L (2005) Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease. J Neurosci 25, 9694-9703. (Pubitemid 41510910)
52. Frangioni JV, Beahm PH, Shifrin V, Jost CA, Neel BG (1992) The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 68, 545-560.
53. Clampit JE, Meuth JL, Smith HT, Reilly RM, Jirousek MR, Trevillyan JM, Rondinone CM (2003) Reduction of protein-tyrosine phosphatase-1B increases insulin signaling in FAO hepatoma cells. Biochem Biophys Res Commun 300, 261-267. (Pubitemid 38375803)
54. Yost C, Farr GH 3rd, Pierce SB, Ferkey DM, Chen MM, Kimelman D (1998) GBP, an inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis. Cell 93 1031-1041. (Pubitemid 28280796)
55. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A (1998) Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phospho-rylation of beta-catenin. EMBO J 17, 1371-1384. (Pubitemid 28105516)
56. Yamamoto H, Kishida S, Uochi T, Ikeda S, Koyama S, Asashima M, Kikuchi A (1998) Axil, a member of the Axin family, interacts with both glycogen synthase kinase 3beta and beta-catenin and inhibits axis formation of Xenopus embryos. Mol Cell Biol 18, 2867-2875. (Pubitemid 28183455)
57. Behrens J, Jerchow BA, Würtele M, Grimm J, Asbrand C, Wirtz R, Kühl M, Wedlich D, Birchmeier W (1998) Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280, 596-599.
58. Takashima A, Murayama M, Murayama O, Kohno T, Honda T, Yasutake K, Nihonmatsu N, Mercken M, Yamaguchi H, Sugihara S, Wolozin B (1998) Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc Natl Acad Sci USA 95, 9637-9641. (Pubitemid 28506284)