Home LiteratureArticle Details
PMID: 9689133 Published · ppublish English Journal Article

Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau.

Takashima A, Murayama M, Murayama O, Kohno T, Honda T, Yasutake K, Nihonmatsu N, Mercken M, Yamaguchi H, Sugihara S, Wolozin B

Abstract

Families bearing mutations in the presenilin 1 (PS1) gene develop Alzheimer's disease. Previous studies have shown that the Alzheimer-associated mutations in PS1 increase production of amyloid beta protein (Abeta1-42). We now show that PS1 also regulates phosphorylation of the microtubule-associated protein tau. PS1 directly binds tau and a tau kinase, glycogen synthase kinase 3beta (GSK-3beta). Deletion studies show that both tau and GSK-3beta bind to the same region of PS1, residues 250-298, whereas the binding domain on tau is the microtubule-binding repeat region. The ability of PS1 to bring tau and GSK-3beta into close proximity suggests that PS1 may regulate the interaction of tau with GSK-3beta. Mutations in PS1 that cause Alzheimer's disease increase the ability of PS1 to bind GSK-3beta and, correspondingly, increase its tau-directed kinase activity. We propose that the increased association of GSK-3beta with mutant PS1 leads to increased phosphorylation of tau.

MeSH Terms
Adult Aged Aged, 80 and over Brain/enzymology,metabolism Calcium-Calmodulin-Dependent Protein Kinases/metabolism Chromatography, Affinity Glycogen Synthase Kinase 3 Glycogen Synthase Kinases Humans Infant, Newborn Membrane Proteins/isolation & purification,metabolism Middle Aged Precipitin Tests Presenilin-1 Substrate Specificity tau Proteins/metabolism
Chemicals
Membrane Proteins PSEN1 protein, human Presenilin-1 tau Proteins Glycogen Synthase Kinases Calcium-Calmodulin-Dependent Protein Kinases Glycogen Synthase Kinase 3
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Takashima A
Laboratory for Alzheimer's Disease, Brain Science Institute, RIKEN, 2-1 Hirosawa, Wako-shi, Saitama 350-01, Japan.
Murayama M
Murayama O
Kohno T
Honda T
Yasutake K
Nihonmatsu N
Mercken M
Yamaguchi H
Sugihara S
Wolozin B
References (48)
48 references, click to expand
  1. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments.
    J Biol Chem. 1986 May 5;261(13):6084-9 PMID: 3084478
  2. Characterization of tau phosphorylation in glycogen synthase kinase-3beta and cyclin dependent kinase-5 activator (p23) transfected cells.
    Biochim Biophys Acta. 1998 Apr 10;1380(2):177-82 PMID: 9565682
  3. Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer's disease.
    J Biochem. 1986 Jun;99(6):1807-10 PMID: 2427509
  4. A68: a major subunit of paired helical filaments and derivatized forms of normal Tau.
    Science. 1991 Feb 8;251(4994):675-8 PMID: 1899488
  5. Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state.
    EMBO J. 1992 Jun;11(6):2131-8 PMID: 1376245
  6. Phosphorylation sites on tau by tau protein kinase I, a bovine derived kinase generating an epitope of paired helical filaments.
    Neurosci Lett. 1992 Dec 14;148(1-2):202-6 PMID: 1284442
  7. Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity.
    Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7789-93 PMID: 8356085
  8. Normal and abnormal biology of the beta-amyloid precursor protein.
    Annu Rev Neurosci. 1994;17:489-517 PMID: 8210185
  9. Association of protein kinase A and protein phosphatase 2B with a common anchoring protein.
    Science. 1995 Jan 6;267(5194):108-11 PMID: 7528941
  10. Proline-directed and non-proline-directed phosphorylation of PHF-tau.
    J Biol Chem. 1995 Jan 13;270(2):823-9 PMID: 7822317
  11. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease.
    Nature. 1995 Jun 29;375(6534):754-60 PMID: 7596406
  12. Candidate gene for the chromosome 1 familial Alzheimer's disease locus.
    Science. 1995 Aug 18;269(5226):973-7 PMID: 7638622
  13. The structure of the presenilin 1 (S182) gene and identification of six novel mutations in early onset AD families.
    Nat Genet. 1995 Oct;11(2):219-22 PMID: 7550356
  14. Presenilins and Alzheimer disease.
    Nat Genet. 1995 Nov;11(3):230-2 PMID: 7581440
  15. Amyloid beta peptide induces cytoplasmic accumulation of amyloid protein precursor via tau protein kinase I/glycogen synthase kinase-3 beta in rat hippocampal neurons.
    Neurosci Lett. 1995 Sep 29;198(2):83-6 PMID: 8592647
  16. Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2719-23 PMID: 8610107
  17. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly.
    Science. 1996 May 17;272(5264):1023-6 PMID: 8638126
  18. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta.
    Neurosci Lett. 1996 Jan 12;203(1):33-6 PMID: 8742040
  19. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo.
    Neuron. 1996 Jul;17(1):181-90 PMID: 8755489
  20. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease.
    Nat Med. 1996 Aug;2(8):864-70 PMID: 8705854
  21. Characterization of human presenilin 1 using N-terminal specific monoclonal antibodies: Evidence that Alzheimer mutations affect proteolytic processing.
    FEBS Lett. 1996 Jul 8;389(3):297-303 PMID: 8766720
  22. In vitro phosphorylation of the cytoplasmic domain of the amyloid precursor protein by glycogen synthase kinase-3beta.
    J Neurochem. 1996 Aug;67(2):699-707 PMID: 8764598
  23. Analysis of phosphorylation of tau with antibodies specific for phosphorylation sites.
    Neurosci Lett. 1995 Dec 29;202(1-2):81-4 PMID: 8787836
  24. The E280A presenilin 1 Alzheimer mutation produces increased A beta 42 deposition and severe cerebellar pathology.
    Nat Med. 1996 Oct;2(10):1146-50 PMID: 8837617
  25. Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3 beta and cyclin-dependent kinase 5, a component of TPK II.
    Acta Neuropathol. 1996 Sep;92(3):232-41 PMID: 8870824
  26. Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1.
    Nature. 1996 Oct 24;383(6602):710-3 PMID: 8878479
  27. Localization of Alzheimer-associated presenilin 1 in transfected COS-7 cells.
    Biochem Biophys Res Commun. 1996 Oct 14;227(2):423-6 PMID: 8878531
  28. Immunocytochemistry of tau phosphoserine 413 and tau protein kinase I in Alzheimer pathology.
    Brain Res. 1996 Oct 21;737(1-2):119-32 PMID: 8930358
  29. Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo.
    Neuron. 1996 Nov;17(5):1005-13 PMID: 8938131
  30. Participation of presenilin 2 in apoptosis: enhanced basal activity conferred by an Alzheimer mutation.
    Science. 1996 Dec 6;274(5293):1710-3 PMID: 8939861
  31. Requirement of the familial Alzheimer's disease gene PS2 for apoptosis. Opposing effect of ALG-3.
    J Biol Chem. 1996 Dec 6;271(49):31025-8 PMID: 8940094
  32. Alzheimer-associated presenilin-2 confers increased sensitivity to apoptosis in PC12 cells.
    FEBS Lett. 1996 Nov 11;397(1):50-4 PMID: 8941712
  33. Antibodies to presenilin proteins detect neurofibrillary tangles in Alzheimer's disease.
    Am J Pathol. 1996 Dec;149(6):1839-46 PMID: 8952521
  34. Nontoxic amyloid beta peptide 1-42 suppresses acetylcholine synthesis. Possible role in cholinergic dysfunction in Alzheimer's disease.
    J Biol Chem. 1997 Jan 24;272(4):2038-41 PMID: 8999897
  35. Regulation of neuronal survival by the serine-threonine protein kinase Akt.
    Science. 1997 Jan 31;275(5300):661-5 PMID: 9005851
  36. Akt signaling: linking membrane events to life and death decisions.
    Science. 1997 Jan 31;275(5300):628-30 PMID: 9019819
  37. Amyloid, the presenilins and Alzheimer's disease.
    Trends Neurosci. 1997 Apr;20(4):154-9 PMID: 9106355
  38. Tau phosphorylation in cells transfected with wild-type or an Alzheimer's disease mutant Presenilin 1.
    Neurosci Lett. 1997 Jan 31;222(2):71-4 PMID: 9111731
  39. Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid beta-peptide: involvement of calcium and oxyradicals.
    J Neurosci. 1997 Jun 1;17(11):4212-22 PMID: 9151738
  40. Presenilin 1 interaction in the brain with a novel member of the Armadillo family.
    Neuroreport. 1997 Apr 14;8(6):1489-94 PMID: 9172160
  41. Neuronal localization of presenilin-1 and association with amyloid plaques and neurofibrillary tangles in Alzheimer's disease.
    J Neurosci. 1997 Jul 1;17(13):5101-7 PMID: 9185547
  42. Presenilin-1 protein expression in familial and sporadic Alzheimer's disease.
    Ann Neurol. 1997 Jun;41(6):742-53 PMID: 9189035
  43. A novel presenilin-1 mutation: increased beta-amyloid and neurofibrillary changes.
    Ann Neurol. 1997 Jun;41(6):809-13 PMID: 9189043
  44. Different effects of Alzheimer-associated mutations of presenilin 1 on its processing.
    Neurosci Lett. 1997 Jun 20;229(1):61-4 PMID: 9224802
  45. Interaction between amyloid precursor protein and presenilins in mammalian cells: implications for the pathogenesis of Alzheimer disease.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8208-13 PMID: 9223340
  46. The role of anchoring protein RACK1 in PKC activation in the ageing rat brain.
    Trends Neurosci. 1997 Sep;20(9):410-5 PMID: 9292970
  47. Presenilin 1 immunostaining using well-characterized antibodies in human tissues.
    Exp Neurol. 1997 Nov;148(1):10-2 PMID: 9398445
  48. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology.
    Proc Natl Acad Sci U S A. 1986 Jul;83(13):4913-7 PMID: 3088567
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-08-04
Pages
9637-41
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC21391
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com