Transgenic mouse and cell culture models demonstrate a lack of mechanistic connection between endoplasmic reticulum stress and tau dysfunction

Journal of Neuroscience Research

Volumn 88, Issue 9, 2010, Pages 1951-1961

  Spatara, M L ^a   Robinson, A S ^a  

^a University of Delaware   (United States)

Author keywords

Alzheimer's disease; Neurofibrillary tangles; Paired helical filaments; PS19; SH SY5Y; Unfolded protein response

Indexed keywords

TAU PROTEIN; THAPSIGARGIN; TUNICAMYCIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; NERVE CELL CULTURE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN VARIANT; SIGNAL TRANSDUCTION; SOLUBILITY; UNFOLDED PROTEIN RESPONSE; WILD TYPE;

ANIMALS; ANTI-BACTERIAL AGENTS; BRAIN; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; GENETIC VARIATION; HUMANS; MICE; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; SOLUBILITY; STRESS, PHYSIOLOGICAL; TAU PROTEINS; THAPSIGARGIN; TUNICAMYCIN; UNFOLDED PROTEIN RESPONSE;

EID: 77953516041     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22359     Document Type: Article

References (52)

1. Alzheimer's Association. 2009. 2009 Alzheimer's disease facts and figures. Alzheimers Dementia vol 5.
2. Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK. 2008. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol Dis 30:400-407.
3. Biedler JL, Roffler-Tarlov S, Schachner M, Freedman LS. 1978. Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 38:3751-3757. (Pubitemid 9045201)
4. Brandt R, Hundelt M, Shahani N. 2005. Tau alteration and neuronal degeneration in tauopathies: mechanisms and models. Biochim Biophys Acta 1739:331-354.
5. Brewster JL, Linseman DA, Bouchard RJ, Loucks FA, Precht TA, Esch EA, Heidenreich KA. 2006. Endoplasmic reticulum stress and trophic factor withdrawal activate distinct signaling cascades that induce glycogen synthase kinase-3 beta and a caspase-9-dependent apoptosis in cerebellar granule neurons. Mol Cell Neurosci 32:242-253.
6. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR. 2000. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33:95-130.
7. Chafekar SM, Hoozemans JJ, Zwart R, Baas F, Scheper W. 2007. Abeta 1-42 induces mild endoplasmic reticulum stress in an aggregation state-dependent manner. Antioxid Redox Signal 9:2245-2254.
8. Cho YM, Jang YS, Jang YM, Chung SM, Kim HS, Lee JH, Jeong SW, Kim IK, Kim JJ, Kim KS, Kwon OJ. 2009. Induction of unfolded protein response during neuronal induction of rat bone marrow stromal cells and mouse embryonic stem cells. Exp Mol Med 41:440-452.
9. Cudna RE, Dickson AJ. 2003. Endoplasmic reticulum signaling as a determinant of recombinant protein expression. Biotechnol Bioeng 81:56-65.
10. Dunnett CW. 1955. A multiple comparison procedure for comparing several treatments with a control. J Am Stat Assoc 50:1096-1121.
11. Ferrari A, Hoerndli F, Baechi T, Nitsch RM, Gotz J. 2003. Beta-amyloid induces paired helical filament-like tau filaments in tissue culture. J Biol Chem 278:40162-40168.
12. Gonzales JC, Gentile CL, Pfaffenbach KT, Wei Y, Wang D, Pagliassotti MJ. 2008. Chemical induction of the unfolded protein response in the liver increases glucose production and is activated during insulin-induced hypoglycaemia in rats. Diabetologia 51:1920-1929.
13. Heifetz A, Keenan RW, Elbein AD. 1979. Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase. Biochemistry 18:2186-2192.
14. 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.
15. 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.
16. 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.
17. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P. 1998. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705.
18. Ishihara T, Higuchi M, Zhang B, Yoshiyama Y, Hong M, Trojanowski JQ, Lee VMY. 2001. Attenuated neurodegenerative disease phenotype in tau transgenic mouse lacking neurofilaments. J Neurosci 21:6026-6035. (Pubitemid 32737736)
19. Jamsa A, Hasslund K, Cowburn RF, Backstrom A, Vasange M. 2004. The retinoic acid and brain-derived neurotrophic factor differentiated SH-SY5Y cell line as a model for Alzheimer's disease-like tau phosphorylation. Biochem Biophys Res Commun 319:993-1000.
20. Jones J, Nivitchanyong T, Giblin C, Ciccarone V, Judd D, Gorfien S, Krag SS, Betenbaugh MJ. 2005. Optimization of tetracycline-responsive recombinant protein production and effect on cell growth and ER stress in mammalian cells. Biotechnol Bioeng 91:722-732.
21. 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.
22. Kim I, Shu CW, Xu W, Shiau CW, Grant D, Vasile S, Cosford ND, Reed JC. 2009. Chemical biology investigation of cell death pathways activated by endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J Biol Chem 284:1593-1603.
23. Lai E, Teodoro T, Volchuk A. 2007. Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology 22:193-201.
24. Lee D, Singaravelu G, Park BJ, Ahnn J. 2007. Differential requirement of unfolded protein response pathway for calreticulin expression in Caenorhabditis elegans. J Mol Biol 372:331-340.
25. Lee VM. 2001. Biomedicine. Tauists and beta-aptists united - well almost! Science 293:1446-1447.
26. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, Lavail MM, Walter P. 2007. IRE1 signaling affects cell fate during the unfolded protein response. Science 318:944-949.
27. Lindholm D, Wootz H, Korhonen L. 2006. ER stress and neurodegenerative diseases. Cell Death Differ 13:385-392.
28. Malhotra JD, Kaufman RJ. 2007. The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18:716-731.
29. Oddo S. 2008. The ubiquitin-proteasome system in Alzheimer's disease. J Cell Mol Med 12:363-373.
30. Perez M, Hernandez F, Gomez-Ramos A, Smith M, Perry G, Avila J. 2002. Formation of aberrant phosphotau fibrillar polymers in neural cultured cells. Eur J Biochem 269:1484-1489.
31. Rahman A, Ting K, Cullen KM, Braidy N, Brew BJ, Guillemin GJ. 2009. The excitotoxin quinolinic acid induces tau phosphorylation in human neurons. PLoS ONE 4:e6344.
32. Resende R, Ferreiro E, Pereira C, Oliveira CR. 2008. ER stress is involved in Abeta-induced GSK-3beta activation and tau phosphorylation. J Neurosci Res 86:2091-2099.
33. Rutkowski DT, Arnold SM, Miller CN, Wu J, Li J, Gunnison KM, Mori K, Sadighi Akha AA, Raden D, Kaufman RJ. 2006. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 4:e374.
34. 2+ transport ATPase by thapsigargin at subnanomolar concentrations. J Biol Chem 266:13503-13506.
35. Scheper W, Hoozemans JJ. 2009. Endoplasmic reticulum protein quality control in neurodegenerative disease: the good, the bad and the therapy. Curr Med Chem 16:615-626.
36. Schroder M, Kaufman RJ. 2005. The mammalian unfolded protein response. Annu Rev Biochem 74:739-789.
37. Selkoe DJ. 2001. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81:741-766.
38. 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.
39. Szegezdi E, Fitzgerald U, Samali A. 2003. Caspase-12 and ER-stress-mediated apoptosis: the story so far. Ann N Y Acad Sci 1010:186-194.
40. Tanaka T, Iqbal K, Trenkner E, Liu DJ, Grundke-Iqbal I. 1995. Abnormally phosphorylated tau in SY5Y human neuroblastoma cells. FEBS Lett 360:5-9.
41. 2+-ATPase. Proc Natl Acad Sci U S A 87:2466-2470.
42. Uberti D, Rizzini C, Spano PF, Memo M. 1997. Characterization of tau proteins in human neuroblastoma SH-SY5Y cell line. Neurosci Lett 235:149-153.
43. Verkhratsky A. 2005. Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85:201-279.
44. Vogelsberg-Ragaglia V, Bruce J, Richter-Landsberg C, Zhang B, Hong M, Trojanowski JQ, Lee VM. 2000. Distinct FTDP-17 missense mutations in tau produce tau aggregates and other pathological phenotypes in transfected CHO cells. Mol Biol Cell 11:4093-4104.
45. Waser M, Mesaeli N, Spencer C, Michalak M. 1997. Regulation of calreticulin gene expression by calcium. J Cell Biol 138:547-557.
46. Wolfe MS. 2009. Tau mutations in neurodegenerative diseases. J Biol Chem 284:6021-6025.
47. Wu J, Kaufman RJ. 2006. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ 13:374-384.
48. Xu YF, Zhang YJ, Zhang AH, Zhang Q, Wu T, Wang JZ. 2004. Attenuation of okadaic acid-induced hyperphosphorylation of cytoskeletal proteins by heat preconditioning and its possible underlying mechanisms. Cell Stress Chaperones 9:304-312.
49. Yoshida H. 2007. ER stress and diseases. FEBS J 274:630-658.
50. 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.
51. Zhang LJ, Chen S, Wu P, Hu CS, Thorne RF, Luo CM, Hersey P, Zhang XD. 2009. Inhibition of MEK blocks GRP78 up-regulation and enhances apoptosis induced by ER stress in gastric cancer cells. Cancer Lett 274:40-46.
52. Zhong J, Iqbal K, Grundke-Iqbal I. 1999. Hyperphosphorylated tau in SY5Y cells: similarities and dissimilarities to abnormally hyperphosphorylated tau from Alzheimer disease brain. FEBS Lett 453:224-228.