Home LiteratureArticle Details
PMID: 9223340 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Interaction between amyloid precursor protein and presenilins in mammalian cells: implications for the pathogenesis of Alzheimer disease.

Xia W, Zhang J, Perez R, Koo EH, Selkoe DJ

Abstract

Mutations in the presenilin 1 (PS1) and presenilin 2 (PS2) genes increase the production of the highly amyloidogenic 42-residue form of amyloid beta-protein (Abeta42) in a variety of cell lines and transgenic mice. To elucidate the molecular mechanism of this effect, wild-type (wt) or mutant PS1 and PS2 genes were stably transfected into Chinese hamster ovary cells expressing endogenous or transfected beta-amyloid precursor protein (APP). By immunoprecipitation/Western blot analysis, APP was consistently found to coimmunoprecipitate with PS1 or PS2 proteins. Several distinct PS1, PS2, or APP antibodies precipitated PS-APP complexes that were detectable by blotting with either APP or PS antibodies. Importantly, complex formation could be detected at endogenous protein levels in nontransfected cells. In various Chinese hamster ovary cell lines, the amounts of APP coprecipitated by PS antibodies were proportional to the expression levels of both APP and PS. APP-PS complexes also were recovered from human 293 and HS683 cells. Full maturation of APP was not required for the interaction; most APP molecules complexed with PS were solely N-glycosylated. Treatment of cells with brefeldin A or incubation at 20 degrees C did not block complex formation, suggesting that the association between APP and PS occurs in part in the endoplasmic reticulum. Complex formation was detected for both wt and mutant PS and APP proteins. Deletion of the APP C-terminal domain did not abrogate complex formation, suggesting that the interaction does not occur in the cytoplasmic domains of the proteins. Our results demonstrate that wt and mutant PS1 and PS2 proteins form complexes with APP in living cells, strongly supporting the hypothesis that mutant PS interacts with APP in a way that enhances the intramembranous proteolysis of the latter by a gamma-secretase cleaving at Abeta42.

MeSH Terms
Alzheimer Disease/genetics,metabolism Amyloid beta-Protein Precursor/metabolism Animals CHO Cells Cricetinae Membrane Proteins/metabolism Presenilin-1 Presenilin-2 Protein Binding Subcellular Fractions/metabolism
Chemicals
Amyloid beta-Protein Precursor Membrane Proteins PSEN1 protein, human PSEN2 protein, human Presenilin-1 Presenilin-2
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Xia W
Department of Neurology, Harvard Medical School, Center for Neurologic Diseases, Brigham and Women's Hospital, Boston, MA 02115, USA.
Zhang J
Perez R
Koo E H
Selkoe D J
References (37)
37 references, click to expand
  1. Sequence of deposition of heterogeneous amyloid beta-peptides and APO E in Down syndrome: implications for initial events in amyloid plaque formation.
    Neurobiol Dis. 1996 Feb;3(1):16-32 PMID: 9173910
  2. 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
  3. Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein and Alzheimer's disease.
    J Neurosci. 1996 Sep 15;16(18):5795-811 PMID: 8795633
  4. Expression and analysis of presenilin 1 in a human neuronal system: localization in cell bodies and dendrites.
    Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9223-8 PMID: 8799182
  5. 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
  6. Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1.
    Nature. 1996 Oct 24;383(6602):710-3 PMID: 8878479
  7. Specific transcellular binding between membrane proteins crucial to Alzheimer disease.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12575-80 PMID: 8901624
  8. The carboxyl termini of beta-amyloid peptides 1-40 and 1-42 are generated by distinct gamma-secretase activities.
    J Biol Chem. 1996 Nov 8;271(45):28655-9 PMID: 8910499
  9. Evidence that the 42- and 40-amino acid forms of amyloid beta protein are generated from the beta-amyloid precursor protein by different protease activities.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13170-5 PMID: 8917563
  10. 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
  11. Protein topology of presenilin 1.
    Neuron. 1996 Nov;17(5):1023-30 PMID: 8938133
  12. 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
  13. The Alzheimer's disease-associated presenilins are differentially phosphorylated proteins located predominantly within the endoplasmic reticulum.
    Mol Med. 1996 Nov;2(6):673-91 PMID: 8972483
  14. Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice.
    Nat Med. 1997 Jan;3(1):67-72 PMID: 8986743
  15. Phosphorylation, subcellular localization, and membrane orientation of the Alzheimer's disease-associated presenilins.
    J Biol Chem. 1997 Feb 7;272(6):3590-8 PMID: 9013610
  16. Alzheimer's disease: genotypes, phenotypes, and treatments.
    Science. 1997 Jan 31;275(5300):630-1 PMID: 9019820
  17. Amyloid precursor protein processing and A beta42 deposition in a transgenic mouse model of Alzheimer disease.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1550-5 PMID: 9037091
  18. The presenilin 2 mutation (N141I) linked to familial Alzheimer disease (Volga German families) increases the secretion of amyloid beta protein ending at the 42nd (or 43rd) residue.
    Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):2025-30 PMID: 9050898
  19. Formation of stable complexes between two Alzheimer's disease gene products: presenilin-2 and beta-amyloid precursor protein.
    Nat Med. 1997 Mar;3(3):328-32 PMID: 9055862
  20. Enhanced production and oligomerization of the 42-residue amyloid beta-protein by Chinese hamster ovary cells stably expressing mutant presenilins.
    J Biol Chem. 1997 Mar 21;272(12):7977-82 PMID: 9065468
  21. 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
  22. Evidence that production and release of amyloid beta-protein involves the endocytic pathway.
    J Biol Chem. 1994 Jul 1;269(26):17386-9 PMID: 8021238
  23. The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease.
    Biochemistry. 1993 May 11;32(18):4693-7 PMID: 8490014
  24. Microtubules, membrane traffic, and cell organization.
    Cell. 1990 Apr 6;61(1):5-7 PMID: 2180584
  25. The Alzheimer amyloid precursor protein. Identification of a stable intermediate in the biosynthetic/degradative pathway.
    J Biol Chem. 1990 Mar 15;265(8):4492-7 PMID: 1968460
  26. Cerebral amyloidosis, ageing and Alzheimer's disease; a contribution from studies on Down's syndrome.
    Neurobiol Aging. 1989 Sep-Oct;10(5):397-9; discussion 412-4 PMID: 2530459
  27. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation.
    Cell. 1983 Aug;34(1):233-43 PMID: 6883510
  28. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo.
    Neuron. 1996 Jul;17(1):181-90 PMID: 8755489
  29. Visualization of A beta 42(43) and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43).
    Neuron. 1994 Jul;13(1):45-53 PMID: 8043280
  30. Cell biology of the amyloid beta-protein precursor and the mechanism of Alzheimer's disease.
    Annu Rev Cell Biol. 1994;10:373-403 PMID: 7888181
  31. Enhanced release of amyloid beta-protein from codon 670/671 "Swedish" mutant beta-amyloid precursor protein occurs in both secretory and endocytic pathways.
    J Biol Chem. 1996 Apr 12;271(15):9100-7 PMID: 8621560
  32. Alzheimer-associated presenilins 1 and 2: neuronal expression in brain and localization to intracellular membranes in mammalian cells.
    Nat Med. 1996 Feb;2(2):224-9 PMID: 8574969
  33. The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway.
    Nat Med. 1995 Dec;1(12):1291-6 PMID: 7489411
  34. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene.
    Nature. 1995 Aug 31;376(6543):775-8 PMID: 7651536
  35. Amyloid beta protein (A beta) deposition: A beta 42(43) precedes A beta 40 in Down syndrome.
    Ann Neurol. 1995 Mar;37(3):294-9 PMID: 7695229
  36. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease.
    Nature. 1995 Jun 29;375(6534):754-60 PMID: 7596406
  37. Candidate gene for the chromosome 1 familial Alzheimer's disease locus.
    Science. 1995 Aug 18;269(5226):973-7 PMID: 7638622
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
1997-07-22
Pages
8208-13
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC21582
Subset
IM
Grants
NIA NIH HHS · R01 AG012749 · United States
NIA NIH HHS · AG12376 · United States
NIA NIH HHS · R01 AG012376 · United States
NIA NIH HHS · P50 AG005134 · United States
NIA NIH HHS · AG12749 · United States
NIA NIH HHS · AG05134 · United States
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