Endoplasmic reticulum stress induces tau pathology and forms a vicious cycle: Implication in Alzheimer's disease pathogenesis

Journal of Alzheimer's Disease

Volumn 28, Issue 4, 2012, Pages 839-854

  Ho, Yuen Shan ^a   Yang, Xifei ^a,d   Lau, Jeffery Chi Fai ^a   Hung, Clara Hui Ling ^a   Wuwongse, Suthicha ^a   Zhang, Qishan ^a   Wang, Jianzhi ^e   Baum, Larry ^f   So, Kwok Fai ^a,b,c   Chang, Raymond Chuen Chung ^a,b,c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d Shenzhen Centre of Disease Control and Prevention   (China)

^e HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^f and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

Alzheimer's disease; ER stress; okadaic acid; tau phosphorylation; thapsigargin

Indexed keywords

CASPASE 3; INITIATION FACTOR 2ALPHA; MESSENGER RNA; MUTANT PROTEIN; OKADAIC ACID; SERINE; TAU PROTEIN; THAPSIGARGIN; THREONINE; X BOX BINDING PROTEIN 1;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN REGION; CELL CULTURE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; TRANSGENIC MOUSE; UNFOLDED PROTEIN RESPONSE;

EID: 84863242250     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-111037     Document Type: Article

References (59)

1. Querfurth HW, LaFerla FM (2010) Alzheimer's disease. N Engl J Med 362, 329-344.
2. Schroder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569, 29-63. (Pubitemid 39643256)
3. Lindholm D, Wootz H, Korhonen L (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13, 385-392.
4. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274. (Pubitemid 29051178)
5. Friedlander R, Jarosch E, Urban J, Volkwein C, Sommer T (2000) A regulatory link between ER-associated protein degradation and the unfolded-protein response. Nat Cell Biol 2, 379-384.
6. Marciniak SJ, Ron D (2006) Endoplasmic reticulum stress signaling in disease. Physiol Rev 86, 1133-1149. (Pubitemid 44521649)
7. Milhavet O, Martindale JL, Camandola S, Chan SL, Gary DS, Cheng A, Holbrook NJ, Mattson MP (2002) Involvement of Gadd153 in the pathogenic action of presenilin-1 mutations. J Neurochem 83, 673-681. (Pubitemid 35231821)
8. Katayama T, Imaizumi K, Honda A, Yoneda T, Kudo T, Takeda M, Mori K, Rozmahel R, Fraser P, George-Hyslop PS, Tohyama M (2001) Disturbed activation of endoplasmic reticulum stress transducers by familial Alzheimer's disease-linked presenilin-1 mutations. J Biol Chem 276, 43446-43454.
9. Hoozemans JJ, van Haastert ES, Eikelenboom P, de Vos RA, Rozemuller JM, Scheper W (2007) Activation of the unfolded protein response in Parkinson's disease. Biochem Biophys Res Commun 354, 707-711. (Pubitemid 46186242)
10. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, Thompson CB (2003) Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 162, 59-69. (Pubitemid 36859535)
11. 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)
12. Rao RV, Castro-Obregon S, Frankowski H, Schuler M, Stoka V, del Rio G, Bredesen DE, Ellerby HM (2002) Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 277, 21836-21842. (Pubitemid 34952336)
13. Kim HJ, Cho HK, Kwon YH (2008) Synergistic induction of ER stress by homocysteine and beta-amyloid in SH-SY5Y cells. J Nutr Biochem 19, 754-761.
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. 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)
16. Hosoi T, Ozawa K (2010) Endoplasmic reticulum stress in disease: Mechanisms and therapeutic opportunities. Clin Sci (Lond) 118, 19-29.
17. Terro F, Czech C, Esclaire F, Elyaman W, Yardin C, Baclet MC, Touchet N, Tremp G, Pradier L, Hugon J (2002) Neurons overexpressing mutant presenilin-1 are more sensitive to apoptosis induced by endoplasmic reticulum-Golgi stress. J Neurosci Res 69, 530-539. (Pubitemid 34831413)
18. Yu MS, Suen KC, Kwok NS, So KF, Hugon J, Chang RC (2006) Beta-amyloid peptides induces neuronal apoptosis via a mechanism independent of unfolded protein responses. Apoptosis 11, 687-700. (Pubitemid 43876839)
19. Lai CS, Preisler J, Baum L, Lee DH, Ng HK, Hugon J, So KF, Chang RC (2009) Low molecular weight Abeta induces collapse of endoplasmic reticulum. Mol Cell Neurosci 41, 32-43.
20. Spatara ML, Robinson AS (2010) Transgenic mouse and cell culture models demonstrate a lack of mechanistic connection between endoplasmic reticulum stress and tau dysfunction. J Neurosci Res 88, 1951-1961.
21. Ho YS, Yu MS, Yang XF, So KF, Yuen WH, Chang RCC (2010) Neuroprotective effects of polysaccharides from wolfberry, the fruits of Lycium barbarum, against homocysteine-induced toxicity in rat cortical neurons. J Alzheimers Dis 19, 813-827.
22. Cheung YT, Zhang NQ, Hung CH, Lai CS, Yu MS, So KF, Chang RCC (2011) Temporal relationship of autophagy and apoptosis in neurons challenged by low molecular weight beta-amyloid peptide. J Cell Mol Med 15, 244-257.
23. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van SM, Gwinn-Hardy K, Paul MM, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin WL, Yen SH, Dickson DW, Davies P, Hutton M (2000) Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25, 402-405. (Pubitemid 32983430)
24. Sahara N, Lewis J, DeTure M, McGowan E, Dickson DW, Hutton M, Yen SH (2002) Assembly of tau in transgenic animals expressing P301L tau: Alteration of phosphorylation and solubility. J Neurochem 83, 1498-1508. (Pubitemid 35477488)
25. Ho YS, Yu MS, Yik SY, So KF, Yuen WH, Chang RC (2009) Polysaccharides from wolfberry antagonizes glutamate excitotoxicity in rat cortical neurons. Cell Mol Neurobiol 29, 1233-1244.
26. Chang RCC, Yu MS, Lai CS (2006) Significance of molecular signaling for protein translation control in neurodegenerative diseases. Neurosignals 15, 249-258.
27. Kins S, Crameri A, Evans DR, Hemmings BA, Nitsch RM, Gotz J (2001) Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J Biol Chem 276, 38193-38200.
28. Kim D, Su J, Cotman CW (1999) Sequence of neurodegeneration and accumulation of phosphorylated tau in cultured neurons after okadaic acid treatment. Brain Res 839, 253-262. (Pubitemid 29416811)
29. Arendt T, Holzer M, Bruckner MK, Janke C, Gartner U (1998) The use of okadaic acid in vivo and the induction of molecular changes typical for Alzheimer's disease. Neuroscience 85, 1337-1340. (Pubitemid 28293435)
30. Vogel J, Anand VS, Ludwig B, Nawoschik S, Dunlop J, Braithwaite SP (2009) The JNK pathway amplifies and drives subcellular changes in tau phosphorylation. Neuropharmacology 57, 539-550.
31. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96. (Pubitemid 34062456)
32. Wang XZ, Lawson B, Brewer JW, Zinszner H, Sanjay A, Mi LJ, Boorstein R, Kreibich G, Hendershot LM, Ron D (1996) Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 16, 4273-4280. (Pubitemid 26251229)
33. Takadera T, Fujibayashi M, Kaniyu H, Sakota N, Ohyashiki T (2007) Caspase-dependent apoptosis induced by thapsigargin was prevented by glycogen synthase kinase-3 inhibitors in cultured rat cortical neurons. Neurochem Res 32, 1336-1342. (Pubitemid 46988194)
34. Fasulo L, Ugolini G, Visintin M, Bradbury A, Brancolini C, Verzillo V, Novak M, Cattaneo A (2000) The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J Neurochem 75, 624-633. (Pubitemid 30485443)
35. Yin H, Kuret J (2006) C-terminal truncation modulates both nucleation and extension phases of tau fibrillization. FEBS Lett 580, 211-215. (Pubitemid 43005338)
36. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140. (Pubitemid 44300242)
37. Sabala P, Czarny M, Woronczak JP, Baranska J (1993) Thapsigargin: Potent inhibitor of Ca2+ transport ATP-ases of endoplasmic and sarcoplasmic reticulum. Acta Biochim Pol 40, 309-319.
38. 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.
39. Morgan D, Munireddy S, Alamed J, DeLeon J, Diamond DM, Bickford P, Hutton M, Lewis J, McGowan E, Gordon MN (2008) Apparent behavioral benefits of tau overexpression in P301L tau transgenic mice. J Alzheimers Dis 15, 605-614.
40. Arendash GW, Lewis J, Leighty RE, McGowan E, Cracchiolo JR, Hutton M, Garcia MF (2004) Multi-metric behavioral comparison of APPsw and P301L models for Alzheimer's disease: Linkage of poorer cognitive performance to tau pathology in forebrain. Brain Res 1012, 29-41. (Pubitemid 38648896)
41. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, Guimaraes A, Yue M, Lewis J, Carlson G, Hutton M, Ashe KH (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 25, 10637-10647. (Pubitemid 41681911)
42. Perreault S, Bousquet O, Lauzon M, Paiement J, Leclerc N (2009) Increased association between rough endoplasmic reticulum membranes and mitochondria in transgenic mice that express P301L tau. J Neuropathol Exp Neurol 68, 503-514.
43. Yoshiyama Y, Higuchi M, Zhang B, Huang SM, Iwata N, Saido TC, Maeda J, Suhara T, Trojanowski JQ, Lee VM (2007) Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53, 337-351. (Pubitemid 46161268)
44. Kim SM, Yoon SY, Choi JE, Park JS, Choi JM, Nguyen T, Kim DH (2010) Activation of eukaryotic initiation factor-2 alpha-kinases in okadaic acid-treated neurons. Neuroscience 169, 1831-1839.
45. Yoon S, Choi J, Yoon J, Huh JW, Kim D (2006) Okadaic acid induces JNK activation, bim overexpression and mitochondrial dysfunction in cultured rat cortical neurons. Neurosci Lett 394, 190-195. (Pubitemid 43144848)
46. Kerokoski P, Suuronen T, Salminen A, Soininen H, Pirttila T (2001) The levels of cdk5 and p35 proteins and tau phosphorylation are reduced during neuronal apoptosis. Biochem Biophys Res Commun 280, 998-1002. (Pubitemid 32924438)
47. Rametti A, Esclaire F, Yardin C, Terro F (2004) Linking alterations in tau phosphorylation and cleavage during neuronal apoptosis. J Biol Chem 279, 54518-54528. (Pubitemid 40053193)
48. Linford NJ, Dorsa DM (2002) 17beta-Estradiol and the phytoestrogen genistein attenuate neuronal apoptosis induced by the endoplasmic reticulum calcium-ATPase inhibitor thapsigargin. Steroids 67, 1029-1040. (Pubitemid 35345166)
49. 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-beta. Nature 403, 98-103. (Pubitemid 30038529)
50. Fu ZQ, Yang Y, Song J, Jiang Q, Liu ZC, Wang Q, Zhu LQWJZ, Tian Q (2010) LiCl attenuates thapsigargin-induced tau hyperphosphorylation by inhibiting GSK-3beta in vivo and in vitro. J Alzheimers Dis 21, 1107-1117.
51. Sagara Y, Inesi G (1991) Inhibition of the sarcoplasmic reticulum Ca2+ transport ATPase by thapsigargin at subnanomolar concentrations. J Biol Chem 266, 13503-13506. (Pubitemid 21907377)
52. Matthews-Roberson TA, Quintanilla RA, Ding H, Johnson GV (2008) Immortalized cortical neurons expressing caspase-cleaved tau are sensitized to endoplasmic reticulum stress induced cell death. Brain Res 1234, 206-212.
53. Meske V, Albert F, Richter D, Schwarze J, Ohm TG (2003) Blockade of HMG-CoA reductase activity causes changes in microtubule-stabilizing protein tau via suppression of geranylgeranylpyrophosphate formation: Implications for Alzheimer's disease. Eur J Neurosci 17, 93-102. (Pubitemid 36098879)
54. Saito T, Konno T, Hosokawa T, Asada A, Ishiguro K, Hisanaga S (2007) p25/cyclin-dependent kinase 5 promotes the progression of cell death in nucleus of endoplasmic reticulum-stressed neurons. J Neurochem 102, 133-140. (Pubitemid 46906270)
55. Ling ZQ, Tian Q, Wang L, Fu ZQ, Wang XC, Wang Q, Wang JZ (2009) Constant illumination induces Alzheimer-like damages with endoplasmic reticulum involvement and the protection of melatonin. J Alzheimers Dis 16, 287-300.
56. Althausen S, Paschen W (2000) Homocysteine-induced changes in mRNA levels of genes coding for cytoplasmic- and endoplasmic reticulum-resident stress proteins in neuronal cell cultures. Brain Res Mol Brain Res 84, 32-40.
57. Oida Y, Shimazawa M, Imaizumi K, Hara H (2008) Involvement of endoplasmic reticulum stress in the neuronal death induced by transient forebrain ischemia in gerbil. Neuroscience 151, 111-119.
58. 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.
59. Wen Y, Yang S, Liu R, Simpkins JW (2004) Transient cerebral ischemia induces site-specific hyperphosphorylation of tau protein. Brain Res 1022, 30-38. (Pubitemid 39194981)