Endogenous Presenilin 1 Redistributes to the Surface of Lamellipodia Upon Adhesion of Jurkat Cells to a Collagen Matrix

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1999 Jul 8

PMID 10393925

Citations 19

Authors

A L Schwarzman

N Singh

M Tsiper

L Gregori

A Dranovsky

M P Vitek

C G Glabe

P H St George-Hyslop

D Goldgaber

Affiliations

Soon will be listed here.

Abstract

Most familial early-onset Alzheimer's disease cases are caused by mutations in the presenilin 1 (PS1) gene. Subcellular localization of the endogenous PS1 is essential for understanding its function, interactions with proteins, and role in Alzheimer's disease. Although numerous studies revealed predominant localization of PS1 to endoplasmic reticulum and Golgi, there are conflicting reports on the localization of PS1 to the cell surface. We found that endogenous PS1 is highly expressed in T lymphocytes (Jurkat cells). Using a variety of methods, we present evidence that endogenous PS1 is localized to the cell surface in addition to intracellular membrane compartments. Moreover, PS1 appeared in high levels on the surface of lamellipodia upon adhesion of the cells to a collagen matrix. The redistribution of PS1 in adhered cells was strikingly similar to that of the well characterized adhesion protein CD44. Cell surface PS1 formed complexes in vivo with actin-binding protein filamin (ABP-280), which is known to form bridges between cell surface receptors and cytoskeleton and mediate cell adhesion and cell motility. Taken together, our results suggest a role of PS1 in cell adhesion and/or cell-matrix interaction.

Citing Articles

Presenilin 1 and Presenilin 2 Target γ-Secretase Complexes to Distinct Cellular Compartments.

Meckler X, Checler F J Biol Chem. 2016; 291(24):12821-12837.

PMID: 27059953 PMC: 4933450. DOI: 10.1074/jbc.M115.708297.

Peptides of presenilin-1 bind the amyloid precursor protein ectodomain and offer a novel and specific therapeutic approach to reduce ß-amyloid in Alzheimer's disease.

Dewji N, Singer S, Masliah E, Rockenstein E, Kim M, Harber M PLoS One. 2015; 10(4):e0122451.

PMID: 25923432 PMC: 4414571. DOI: 10.1371/journal.pone.0122451.

Circulating anti-filamin C autoantibody as a potential serum biomarker for low-grade gliomas.

Adachi-Hayama M, Adachi A, Shinozaki N, Matsutani T, Hiwasa T, Takiguchi M BMC Cancer. 2014; 14:452.

PMID: 24946857 PMC: 4094678. DOI: 10.1186/1471-2407-14-452.

Alzheimer's disease-linked presenilin mutation (PS1M146L) induces filamin expression and γ-secretase independent redistribution.

Lu Q, Ding K, Frosch M, Jones S, Wolfe M, Xia W J Alzheimers Dis. 2010; 22(1):235-45.

PMID: 20847418 PMC: 3813954. DOI: 10.3233/JAD-2010-100585.

Presenilin mutations linked to familial Alzheimer's disease cause an imbalance in phosphatidylinositol 4,5-bisphosphate metabolism.

Landman N, Jeong S, Shin S, Voronov S, Serban G, Kang M Proc Natl Acad Sci U S A. 2006; 103(51):19524-9.

PMID: 17158800 PMC: 1748258. DOI: 10.1073/pnas.0604954103.

References

Dewji N, Singer S . Cell surface expression of the Alzheimer disease-related presenilin proteins. Proc Natl Acad Sci U S A. 1997; 94(18):9926-31. PMC: 23298. DOI: 10.1073/pnas.94.18.9926. View

Howell M, Diveley J, Lundeen K, Esty A, Winters S, Carlo D . Limited T-cell receptor beta-chain heterogeneity among interleukin 2 receptor-positive synovial T cells suggests a role for superantigen in rheumatoid arthritis. Proc Natl Acad Sci U S A. 1991; 88(23):10921-5. PMC: 53044. DOI: 10.1073/pnas.88.23.10921. View

Levitan D, Doyle T, BROUSSEAU D, Lee M, Thinakaran G, Slunt H . Assessment of normal and mutant human presenilin function in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1996; 93(25):14940-4. PMC: 26241. DOI: 10.1073/pnas.93.25.14940. View

Busciglio J, Hartmann H, Lorenzo A, Wong C, Baumann K, Sommer B . Neuronal localization of presenilin-1 and association with amyloid plaques and neurofibrillary tangles in Alzheimer's disease. J Neurosci. 1997; 17(13):5101-7. PMC: 6573321. View

De Fea K, Nakahara D, Calayag M, Yost C, Mirels L, Prusiner S . Determinants of carboxyl-terminal domain translocation during prion protein biogenesis. J Biol Chem. 1994; 269(24):16810-20. View

Wu D, Cederbaum A . Presence of functionally active cytochrome P-450IIE1 in the plasma membrane of rat hepatocytes. Hepatology. 1992; 15(3):515-24. DOI: 10.1002/hep.1840150326. View

Lesley J, HYMAN R, Kincade P . CD44 and its interaction with extracellular matrix. Adv Immunol. 1993; 54:271-335. DOI: 10.1016/s0065-2776(08)60537-4. View

Altin J, Pagler E . A one-step procedure for biotinylation and chemical cross-linking of lymphocyte surface and intracellular membrane-associated molecules. Anal Biochem. 1995; 224(1):382-9. DOI: 10.1006/abio.1995.1054. View

Cribbs D, Chen L, Bende S, Laferla F . Widespread neuronal expression of the presenilin-1 early-onset Alzheimer's disease gene in the murine brain. Am J Pathol. 1996; 148(6):1797-806. PMC: 1861636. View

10.

Weidemann A, Paliga K, Durrwang U, Czech C, Evin G, Masters C . Formation of stable complexes between two Alzheimer's disease gene products: presenilin-2 and beta-amyloid precursor protein. Nat Med. 1997; 3(3):328-32. DOI: 10.1038/nm0397-328. View

11.

Aruffo A, Stamenkovic I, Melnick M, Underhill C, Seed B . CD44 is the principal cell surface receptor for hyaluronate. Cell. 1990; 61(7):1303-13. DOI: 10.1016/0092-8674(90)90694-a. View

12.

von Boehmer H . T-call development: is notch a key player in lineage decisions?. Curr Biol. 1997; 7(5):R308-10. DOI: 10.1016/s0960-9822(06)00145-x. View

13.

Goodman C . Mechanisms and molecules that control growth cone guidance. Annu Rev Neurosci. 1996; 19:341-77. DOI: 10.1146/annurev.ne.19.030196.002013. View

14.

Zhang W, Han S, McKeel D, Goate A, Wu J . Interaction of presenilins with the filamin family of actin-binding proteins. J Neurosci. 1998; 18(3):914-22. PMC: 2042137. View

15.

Matsudaira P . Actin crosslinking proteins at the leading edge. Semin Cell Biol. 1994; 5(3):165-74. DOI: 10.1006/scel.1994.1021. View

16.

VON DIPPE P, Amoui M, STELLWAGEN R, Levy D . The functional expression of sodium-dependent bile acid transport in Madin-Darby canine kidney cells transfected with the cDNA for microsomal epoxide hydrolase. J Biol Chem. 1996; 271(30):18176-80. DOI: 10.1074/jbc.271.30.18176. View

17.

Doan A, Thinakaran G, Borchelt D, Slunt H, Ratovitsky T, Podlisny M . Protein topology of presenilin 1. Neuron. 1996; 17(5):1023-30. DOI: 10.1016/s0896-6273(00)80232-9. View

18.

Del Pozo M, Cabanas C, Montoya M, Ager A, Sanchez-Mateos P, Sanchez-Madrid F . ICAMs redistributed by chemokines to cellular uropods as a mechanism for recruitment of T lymphocytes. J Cell Biol. 1997; 137(2):493-508. PMC: 2139764. DOI: 10.1083/jcb.137.2.493. View

19.

Van Broeckhoven C . Presenilins and Alzheimer disease. Nat Genet. 1995; 11(3):230-2. DOI: 10.1038/ng1195-230. View

20.

Xia W, Zhang J, Perez R, Koo E, Selkoe D . 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; 94(15):8208-13. PMC: 21582. DOI: 10.1073/pnas.94.15.8208. View