Increased levels of tau protein in SH-SY5Y cells after treatment with cholinesterase inhibitors and nicotinic agonists

Journal of Neurochemistry

Volumn 74, Issue 2, 2000, Pages 777-784

  Hellström Lindahl, Ewa ^a   Moore, Helen ^a   Nordberg, Agneta ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Alzheimer's disease; Cholinesterase inhibitors; Nicotine; Nicotinic receptors; SH SY5Y cells; Tau

Indexed keywords

CHOLINESTERASE INHIBITOR; DONEPEZIL; EPIBATIDINE; GALANTAMINE; MECAMYLAMINE; NICOTINIC AGENT; RIVASTIGMINE; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CELL TRANSPORT; CHOLINERGIC TRANSMISSION; DRUG EFFECT; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; SENILE PLAQUE;

ALKALINE PHOSPHATASE; ATROPINE; CALCIUM; CHOLINESTERASE INHIBITORS; CULTURE MEDIA; HUMANS; NEUROBLASTOMA; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; TAU PROTEINS; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 2542509442     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.740777.x     Document Type: Article

References (56)

1. Adamec E., Mercken M., Beerman M. L., Didier M., and Nixon R. A. (1997) Acute rise in the concentration of free cytoplasmic calcium leads to dephosphorylation of the microtubule-associated protein tau. Brain Res. 757, 93-101.
2. Bencherif M., Fowler K., Lukas R., and Lipiello P. (1995) Mechanisms of up-regulation of neuronal nicotinic acetylcholine receptors in clonal cell lines and primary cultures of fetal rat brain. J. Pharmacol. Exp. Ther. 275, 987-994.
3. 3H]nicotine binding sites in human brain. J. Neurochem. 50, 1243-1247.
4. Billingsley M. L. and Kincaid R. L. (1997) Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem. J. 323, 577-591.
5. Binder L. I., Frankfurter A., and Rebhun L. I. (1985) The distribution of tau polypeptides in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378.
6. Burack M. A. and Halpain S. (1996) Site-specific regulation of Alzheimer-like tau phosphorylation in living neurons. Neuroscience 72, 167-184.
7. Buxbaum J. D., Oishi M., Chen H. I., Pinkas-Kramarski R., Jaffe E. A., Gandy S. E., and Greengard P. (1992) Cholinergic agonists and interleukin-1 regulate processing and secretion of the Alzheimer beta/A4 amyloid protein precursor. Proc. Natl. Acad. Sci. USA 889, 10075-10078.
8. Chavez-Noriega L. E., Crona J. H., Washburn M. S., Urrutia A., Elliott K. J., and Johnson E. C. (1997) Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors hα2β2, hα2β4, hα3β2, hα3β4, hα4β2, hα4β4 and hα7 expressed in Xenopus oocytes. J. Pharmacol. Exp. Ther. 280, 346-356.
9. Eilers H., Schaeffer E., Bickler P. E., and Forsayeth J. R. (1997) Functional deactivation of the major neuronal nicotinic receptor caused by nicotine and a protein kinase C-dependent mechanism. Mol. Pharmacol. 52, 1105-1112.
10. Esclaire F., Lesort M., Blanchard C., and Hugon J. (1997) Glutamate toxicity enhances tau gene expression in neuronal cultures. J. Neurosci. Res. 49, 309-318.
11. Fenster C. P., Whitworth T. L., Sheffield E. B., Quick M. W., and Lester R. A. J. (1999) Upregulation of surface α4β2 nicotinic receptors is initiated by receptor desensitization after chronic exposure to nicotine. J. Neurosci. 19, 4804-4814.
12. Goedert M. and Vanmechelen E. (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci. Lett. 189, 167-170.
13. Goedert M., Jakes R., Crowther R. A., Cohen P., Vanmechelen E., Vandermeeren M., and Cras P. (1994) Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau. Biochem. J. 301, 871-877.
14. Hellström-Lindahl E., Mousavi M., Zhang X., Ravid R., and Nordberg A. (1999) Regional distribution of nicotinic receptor subunit mRNAs in human brain: comparison between Alzheimer and normal brain. Mol. Brain Res. 66, 94-103.
15. Imahori K. and Uchida T. (1997) Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J. Biochem. (Tokyo) 121, 179-188.
16. Johnson G. V. W. and Hartigan J. A. (1998) Tau protein in normal and Alzheimer's disease brain: an update. Alzheimers Dis. Rev. 3, 125-141.
17. Kiefer-Day J. S., Abdallah E.-S., Forray C., Lee N. H., Kim O. N., and El-Fakahany E. E. (1993) Effects of tacrine on brain muscarinic-receptor-mediated second-messenger signals. Pharmacology 47, 98-110.
18. Lew G. (1992) Microtubular tau protein after cocaine treatment in cultured SH-SY5Y human neuroblastoma. Gen. Pharmacol. 23, 1111-1113.
19. Litersky J. M. and Johnson G. V. W. (1995) Phosphorylation of τ in situ: inhibition of calcium-dependent proteolysis. J. Neurochem. 65, 903-911.
20. Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
21. Lukas R., Norman S., and Lucero L. (1993) Characterization of nicotinic acetylcholine receptors expressed by cells of the SH-SY5Y human neuroblastoma clonal line. Mol. Cell. Neurosci. 4, 1-12.
22. Maelicke A., Schrattenholz A., Storch A., Schröder B., Gutbrod O., Methfessel C., Weber K.-H., Pereira E. E., Alkondon M., and Albuquerque E. X. (1995) Noncompetitive agonism at nicotinic acetylcholine receptors; functional significance for CNS signal transduction. J. Recept. Signal Transduct. Res. 15, 333-353.
23. Marutle A., Warpman U., Bogdanovic N., Lannfelt L., and Nordberg A. (1999) Neuronal nicotinic receptor deficits in Alzheimer patients with the Swedish amyloid precursor protein 670/671 mutation. J. Neurochem. 72, 1161-1169.
24. Matsuo E. S., Shin R.-W., Billingsley M. L., Van de Voorde A., O'Connor M., Trojanowski J. Q., and Lee V. M.-Y. (1994) Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13, 989-1002.
25. 2+ influx in cultured hippocampal neurons. Neuron 2, 105-117.
26. Nilsson-Håkansson L., Lai Z., and Nordberg A. (1990) Tetrahydroaminoacridine induces opposite changes in muscarinic and nicotinic receptors in rat brain. Eur. J. Pharmacol. 186, 301-305.
27. Nitsch R. M., Slack B. E., Wurtman R. J., and Growdon J. H. (1992) Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science 258, 304-307.
28. Nordberg A. (1992) Neuroreceptor changes in Alzheimer disease. Cerebrovasc. Brain Metab. Rev. 4, 303-328.
29. Nordberg A. and Svensson A.-L. (1998) Cholinesterase inhibitors in the treatment of Alzheimer's disease. A comparison of tolerability and pharmacology. Drug Safety 19, 465-480.
30. Nordberg A., Lilja A., Lundqvist H., Hartwig P., Amberla K., Viitanen M., Warpman U., Johansson M., Hellström-Lindahl E., Bjurling P., Fasth K.-J., Långström B., and Winblad B. (1992) Tacrine restores cholinergic nicotinic receptors and glucose metabolism in Alzheimer patients as visualized by positron emission tomography. Neurobiol. Aging 13, 747-758.
31. Olale F, Gerzanich V., Kuryatov A., Wang F., and Lindstrom J. (1997) Chronic nicotine exposure differentially affects the function of human α3, α4, and α7 neuronal nicotinic receptor subtypes. J. Pharmacol. Exp. Ther. 283, 675-683.
32. Pauly J., Marks M., Robinson S., Kamp J. V. D., and Collins A. (1996) Chronic nicotine and mecamylamine treatment increase brain nicotinic receptor binding sites without changing α4 or β2 mRNA levels. J. Pharmacol. Exp. Ther. 278, 361-369.
33. Peng X., Gerzanich V., Anand R., Whiting P., and Lindstrom J. (1994) Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol. Pharmacol. 46, 523-530.
34. Peng X., Gerzanich V., Anand R., Wang F., and Lindstrom J. (1997) Chronic nicotine treatment up-regulates α3 and α7 acetylcholine receptor subtypes expressed by the human neuroblastoma cell line SH-SY5Y. Mol. Pharmacol. 51, 776-784.
35. Pereira E. F. R., Reinhardt-Maelicke S., Schrattenholz A., Maelicke A., and Albuquerque E. X. (1993) Identification and functional characterization of a new agonist site on nicotinic acetylcholine receptors of cultured hippocampal neurons. J. Pharmacol. Exp. Ther. 265, 1474-1491.
36. Pereira E. F. R., Alkondon M., Reinhardt S., Maelicke A., Peng X., Lindstrom J., Whiting J., and Albuquerque E. X. (1994) Physostigmine and galanthamine characterize the presence of a novel binding site on the α4β2 subtype of neuronal nicotinic acetylcholine receptors stably expressed in fibroblast cells. J. Pharmacol Exp. Ther. 270, 768-778.
37. Pope W. B., Lambert M. P., Leypold B., Seupaul R., Sletten L., Krafft G., and Klein W. (1994) Microtubule-associated protein tau is hyperphosphorylated during mitosis in the human neuroblastoma cell line SH-SY5Y. Exp. Neurol. 126, 185-194.
38. 1 muscarinic acetylcholine receptor regulates τ phosphorylation in transfected PC12 cells. J. Neurochem. 66, 877-880.
39. Schrattenholz A., Pereira E. F. R., Roth U., Weber K.-H., and Albuquerque E. X. (1996) Agonist responses of neuronal nicotinic acetylcholine receptors are potentiated by a novel class of allosterically acting ligands. Mol. Pharmacol. 49, 1-6.
40. Shea T. B., Spencer M. J., Beermann M. L., Cressman C. M., and Nixon R. A. (1996) Calcium influx into human neuroblastoma cells induces ALZ-50 immunoreactivity: involvement of calpain-mediated hydrolysis of protein kinase C. J. Neurochem. 66, 1539-1549.
41. Shea T. B., Prabhakar S., and Ekinci F. (1997) β-Amyloid and ionophore A23187 evoke tau hyperphosphorylation by distinct intracellular pathways: differential involvement of the calpain/protein kinase C system. J. Neurosci. Res. 49, 759-768.
42. Sindou P., Lesort M., Couratier P., Yardin C., Esclaire F., and Hugon J. (1994) Glutamate increases tau phosphorylation in primary neuronal cultures from fetal rat cerebral cortex. Brain Res. 646, 124-128.
43. Smith C. J., Anderton B. H., Davis D. R., and Gallo J.-M. (1995) Tau isoform expression and phosphorylation state during differentiation of cultured neuronal cells. FEBS Lett. 375, 243-248.
44. Spillantini M. G. and Goedert M. (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci. 21, 428-433.
45. Strittmatter W., Saunders A. M., Schmechel D. E., Pericak-Vance M. A., Enghild J., Salvesen G. S., and Roses A. D. (1993) Apolipoprotein E: high avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. USA 90, 1977-1981.
46. Svensson A.-L. and Nordberg A. (1996) Tacrine interacts with an allosteric activator site on α4β2 nAChRs in M10 cells. Neuroreport 7, 2201-2205.
47. Svensson A.-L. and Nordberg A. (1997) Interaction of tacrine, galanthamine, NXX-066 and E2020 with neuronal α4β2 nicotinic receptors expressed in fibroblast cells, in Alzheimer's Disease: Biology, Diagnosis and Therapeutics (Iqbal K., Winblad B., Nishimura T., Taked M., and Wisniewski H. M., eds), pp. 753-758, John Wiley & Sons, New York.
48. Svensson A.-L., Zhang X., and Nordberg A. (1996) Biphasic effect of tacrine on acetylcholine release in rat brain via M1 and M2 receptors. Brain Res. 726, 207-212.
49. Tanaka T., Iqbal K., Trenkner E., Lie D. J., and Grundke-Iqbal I. (1995) Abnormally phosphorylated tau in SY5Y human neuroblastoma cells. FEBS Lett. 360, 5-9.
50. Trojanowski J. Q. and Lee V. M.-Y. (1993) Phosphorylation of paired helical filament tau in Alzheimer's disease neurofibrillary lesions: focusing on phosphatases. FASEB J. 9, 1570-1576.
51. Vincent I., Rosado M., Kim E., and Davies P. (1994) Increased production of paired helical filament epitopes in a cell culture system reduces the turnover of τ. J. Neurochem. 62, 715-723.
52. Wagstaff A. J. and McTavish D. (1994) Tacrine. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic efficacy in Alzheimer's disease. Drugs Aging 4, 510-540.
53. Warpman U., Friberg L., Gillespie A., Hellström-Lindahl E., Zhang X., and Nordberg A. (1998) Regulation of nicotinic receptor subtypes following chronic nicotinic agonist exposure in M10 and SH-SY5Y neuroblastoma cells. J. Neurochem. 70, 2028-2037.
54. Whiteaker P., Sharples C. G. V., and Wonnacott S. (1998) Agonist-induced up-regulation of α4β2 nicotinic acetylcholine receptors in M10 cells: pharmacological and spatial definition. Mol. Pharmacol. 53, 950-962.
55. Wolf B. A., Wertkin A. M., Jolly Y. C., Yasuda R. P., Wolfe B. B., Konrad R. J., Manning D., Ravi S., Williamson J. R., and Lee V. M.-Y. (1995) Muscarinic regulation of Alzheimer's disease amyloid precursor protein secretion and amyloid β-protein production in human NT2N cells. J. Biol. Chem. 270, 4916-4922.
56. Zhang Z., Gong Z-H., Hellström-Lindahl E., and Nordberg A. (1995) Regulation of α4β2 nicotinic acetylcholine receptors in M10 cells following treatment with nicotinic agents. Neuroreport 6, 313-317.