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PMID: 11226248 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Presenilin-1 binds cytoplasmic epithelial cadherin, inhibits cadherin/p120 association, and regulates stability and function of the cadherin/catenin adhesion complex.

Baki L, Marambaud P, Efthimiopoulos S, Georgakopoulos A, Wen P, Cui W, Shioi J, Koo E, Ozawa M, Friedrich VL, Robakis NK

Abstract

Here we show that presenilin-1 (PS1), a protein involved in Alzheimer's disease, binds directly to epithelial cadherin (E-cadherin). This binding is mediated by the large cytoplasmic loop of PS1 and requires the membrane-proximal cytoplasmic sequence 604-615 of mature E-cadherin. This sequence is also required for E-cadherin binding of protein p120, a known regulator of cadherin-mediated cell adhesion. Using wild-type and PS1 knockout cells, we found that increasing PS1 levels suppresses p120/E-cadherin binding, and increasing p120 levels suppresses PS1/E-cadherin binding. Thus PS1 and p120 bind to and mutually compete for cellular E-cadherin. Furthermore, PS1 stimulates E-cadherin binding to beta- and gamma-catenin, promotes cytoskeletal association of the cadherin/catenin complexes, and increases Ca(2+)-dependent cell-cell aggregation. Remarkably, PS1 familial Alzheimer disease mutant DeltaE9 increased neither the levels of cadherin/catenin complexes nor cell aggregation, suggesting that this familial Alzheimer disease mutation interferes with cadherin-based cell-cell adhesion. These data identify PS1 as an E-cadherin-binding protein and a regulator of E-cadherin function in vivo.

MeSH Terms
Animals Binding, Competitive Cadherins/metabolism Cell Adhesion Cell Line Cytoplasm/metabolism Cytoskeletal Proteins/metabolism Cytoskeleton/metabolism Epithelial Cells/metabolism Membrane Proteins/metabolism Mice Presenilin-1 Protein Binding Trans-Activators beta Catenin
Chemicals
CTNNB1 protein, mouse Cadherins Cytoskeletal Proteins Membrane Proteins Presenilin-1 Trans-Activators beta Catenin
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Baki L
Department of Psychiatry, Fishberg Research Center for Neurobiology, Mount Sinai School of Medicine, One Gustave Levy Place, New York, NY 10029, USA.
Marambaud P
Efthimiopoulos S
Georgakopoulos A
Wen P
Cui W
Shioi J
Koo E
Ozawa M
Friedrich V L
Robakis N K
References (36)
36 references, click to expand
  1. E-cadherin mediates adhesion and suppresses cell motility via distinct mechanisms.
    J Cell Sci. 1997 Feb;110 ( Pt 3):345-56 PMID: 9057087
  2. Presenilin-1-immunoreactive neurons are preserved in late-onset Alzheimer's disease.
    Am J Pathol. 1997 Feb;150(2):429-36 PMID: 9033258
  3. Presenilin proteins undergo heterogeneous endoproteolysis between Thr291 and Ala299 and occur as stable N- and C-terminal fragments in normal and Alzheimer brain tissue.
    Neurobiol Dis. 1997;3(4):325-37 PMID: 9173929
  4. Appican expression induces morphological changes in C6 glioma cells and promotes adhesion of neural cells to the extracellular matrix.
    J Neurosci. 1997 Jul 1;17(13):4987-93 PMID: 9185536
  5. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein.
    Nature. 1998 Jan 22;391(6665):387-90 PMID: 9450754
  6. Alzheimer's disease: a re-examination of the amyloid hypothesis.
    Trends Neurosci. 1998 Jan;21(1):15-9 PMID: 9464679
  7. A causal role for E-cadherin in the transition from adenoma to carcinoma.
    Nature. 1998 Mar 12;392(6672):190-3 PMID: 9515965
  8. Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization.
    J Cell Biol. 1998 Mar 23;140(6):1475-84 PMID: 9508779
  9. A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation.
    Neuron. 1998 Jun;20(6):1165-75 PMID: 9655504
  10. Direct association of presenilin-1 with beta-catenin.
    FEBS Lett. 1998 Aug 14;433(1-2):73-7 PMID: 9738936
  11. The membrane-proximal region of the E-cadherin cytoplasmic domain prevents dimerization and negatively regulates adhesion activity.
    J Cell Biol. 1998 Sep 21;142(6):1605-13 PMID: 9744888
  12. Differential molecular interactions of beta-catenin and plakoglobin in adhesion, signaling and cancer.
    Curr Opin Cell Biol. 1998 Oct;10(5):629-39 PMID: 9818174
  13. Presenilins interact with armadillo proteins including neural-specific plakophilin-related protein and beta-catenin.
    J Neurochem. 1999 Mar;72(3):999-1008 PMID: 10037471
  14. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain.
    Nature. 1999 Apr 8;398(6727):518-22 PMID: 10206645
  15. p120(ctn) binds to the membrane-proximal region of the E-cadherin cytoplasmic domain and is involved in modulation of adhesion activity.
    J Biol Chem. 1999 Jul 23;274(30):21409-15 PMID: 10409703
  16. Neuroplasticity failure in Alzheimer's disease: bridging the gap between plaques and tangles.
    Neuron. 1999 Nov;24(3):521-9 PMID: 10595506
  17. Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion.
    J Cell Biol. 2000 Jan 10;148(1):189-202 PMID: 10629228
  18. Presenilin-1 forms complexes with the cadherin/catenin cell-cell adhesion system and is recruited to intercellular and synaptic contacts.
    Mol Cell. 1999 Dec;4(6):893-902 PMID: 10635315
  19. Regulation of cadherin adhesive activity.
    J Cell Biol. 2000 Feb 7;148(3):399-404 PMID: 10662767
  20. Molecular modification of N-cadherin in response to synaptic activity.
    Neuron. 2000 Jan;25(1):93-107 PMID: 10707975
  21. The p120 catenin family: complex roles in adhesion, signaling and cancer.
    J Cell Sci. 2000 Apr;113 ( Pt 8):1319-34 PMID: 10725216
  22. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity.
    Genes Dev. 2000 May 15;14(10):1169-80 PMID: 10817752
  23. Cell binding function of E-cadherin is regulated by the cytoplasmic domain.
    EMBO J. 1988 Dec 1;7(12):3679-84 PMID: 3061804
  24. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species.
    EMBO J. 1989 Jun;8(6):1711-7 PMID: 2788574
  25. Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin.
    Cell Regul. 1989 Nov;1(1):37-44 PMID: 2519616
  26. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain.
    Cell. 1992 Apr 17;69(2):225-36 PMID: 1568244
  27. Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells.
    J Cell Biol. 1994 Jun;125(6):1341-52 PMID: 8207062
  28. Assembly of the cadherin-catenin complex in vitro with recombinant proteins.
    J Cell Sci. 1994 Dec;107 ( Pt 12):3655-63 PMID: 7706414
  29. Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex.
    Proc Natl Acad Sci U S A. 1995 May 23;92(11):5067-71 PMID: 7761449
  30. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease.
    Nature. 1995 Jun 29;375(6534):754-60 PMID: 7596406
  31. Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8813-7 PMID: 7568023
  32. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo.
    Neuron. 1996 Jul;17(1):181-90 PMID: 8755489
  33. Identification and neuron specific expression of the S182/presenilin I protein in human and rodent brains.
    J Neurosci Res. 1996 Aug 1;45(3):308-20 PMID: 8841992
  34. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo.
    Neuron. 1996 Nov;17(5):837-48 PMID: 8938117
  35. Secreted glypican binds to the amyloid precursor protein of Alzheimer's disease (APP) and inhibits APP-induced neurite outgrowth.
    J Biol Chem. 1996 Dec 6;271(49):31215-21 PMID: 8940123
  36. Skeletal and CNS defects in Presenilin-1-deficient mice.
    Cell. 1997 May 16;89(4):629-39 PMID: 9160754
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
2001-02-27
Pages
2381-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC30147
Subset
IM
Grants
NIA NIH HHS · AG-08200 · United States
NIA NIH HHS · AG-17926 · United States
NIA NIH HHS · R01 AG008200 · United States
NIA NIH HHS · R37 AG017926 · United States
NIA NIH HHS · P50 AG005138 · United States
NIA NIH HHS · AG-05138 · United States
NIA NIH HHS · R01 AG017926 · United States
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