Subcellular localization of presenilins: Association with a unique membrane pool in cultured cells

Neurobiology of Disease

Volumn 7, Issue 2, 2000, Pages 99-117

  Kim, Seong Hun ^a   Lah, James J ^b   Thinakaran, Gopal ^a   Levey, Allan ^b   Sisodia, Sangram S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRESENILIN 1; PRESENILIN 2;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; MOUSE; NERVE CELL; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL;

EID: 0034098993     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1006/nbdi.1999.0280     Document Type: Article

References (67)

1. Nat. Genet. 11:1995;219-222.
2. Balch W. E., Rothman J. E. Characterization of protein transport between successive compartments of the Golgi apparatus: Asymmetric properties of donor and acceptor activities in a cell free system. Arch. Biochem. Biophys. 240:1985;413-425.
3. Baumeister R., Leimer U., Zweckbronner I., Jakubek C., Grunberg J., Haass C. Human presenilin-1, but not familial Alzheimer's disease (FAD) mutants, facilitate Caenorhabditis elegans Notch signalling independently of proteolytic processing. Genes Funct. 1:1997;149-159.
4. Bole D. G., Hendershot L. M., Kearney J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J. Cell Biol. 102:1986;1558-1566.
5. Borchelt D. R., Thinakaran G., Eckman C. B., Lee M. K., Davenport F., Ratovitsky T., Prada C.-M., Kim G., Seekins S., Yager D., Slunt H. H., Wang R., Seeger M., Levey A. I., Gandy S. E., Copeland N. G., Jenkins N. A., Price D. L., Younkin S. G., Sisodia S. S. Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ1-42/1-40 ratio in vitro and in vivo. Neuron. 17:1996;1005-1013.
6. Borchelt D. R., Ratovitski T., van Lare J., Lee M. K., Gonzales V., Jenkins N. A., Copeland N. G., Price D. L., Sisodia S. S. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron. 19:1997;939-945.
7. Brewer G. J., Torriceli J. R., Evege E. K., Price P. J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35:1993;567-576.
8. Busciglio J., Hartmann H., Lorenzo A., Wong C., Baumann K., Sommer B., Staufenbiel M., Yankner B. A. Neuronal localization of presenilin-1 and association with amyloid plaques and neurofibrillary tangles in Alzheimer's disease. J. Neurosci. 17:1997;5101-5107.
9. Capell A., Grunberg J., Pesold B., Diehlmann A., Citron M., Nixon R., Beyreuther K., Selkoe D. J., Haass C. The proteolytic fragments of the Alzheimer's disease associated presenilin-1 form heterodimers and occur as a 100-150-kDa molecular mass complex. J. Biol. Chem. 273:1998;3205-3211.
10. Capell A., Saffrich R., Olivo J. C., Meyn L., Walter J., Grunberg J., Mathews P., Nixon R., Dotti C., Haass C. Cellular expression and proteolytic processing of presenilin proteins is developmentally regulated during neuronal differentiation. J. Neurochem. 69:1997;2432-2440.
11. Citron M., Westaway D., Xia W., Carlson G., Diehl T., Levesque G., Johnson-Wood K., Lee M., Seubert P., Davis A., Kholodenko D., Motter R., Sherrington R., Perry B., Yao H., Strome R., Lieberburg I., Rommens J., Kim S., Schenk D., Fraser P., St. George Hyslop P., Selkoe D. J. Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat. Med. 3:1997;67-72.
12. Cole N. B., Sciaky N., Marotta A., Song J., Lippincort-Schwartz J. Golgi dispersal during microtubule disruption: Regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell. 7:1996;631-650.
13. Cook D. G., Sung J. C., Golde T. E., Felsenstein K. M., Wojczyk B. S., Tanzi R. E., Trojanowski J. Q., Lee V. M.-Y., Doms R. W. Expression and analysis of presenilin 1 in a human neuronal system: Localization in cell bodies and dendrites. Proc. Natl. Acad. Sci. USA. 93:1996;9223-9228.
14. Culvenor J. G., Maher F., Evin G., Malchiodi-Albedi F., Cappai R., Underwood J. R., Davis J. B., Karran E. H., Roberts G., Beyreuther K., Masters C. L. Alzheimer disease-associated presenilin-1 in neuronal cells; evidence for localization to the endoplasmic reticulum-Golgi intermediate compartment. J. Neurosci. Res. 47:1997;719-731.
15. Dascher C., Matteson J., Balch W. E. Syntaxin 5 regulates endoplasmic reticulum to Golgi transport. J. Biol. Chem. 269:1994;29363-29366.
16. DeStrooper B., Beullens M., Contreras B., Levesque L., Craessaerts K., Cordell B., Moechars D., Bollen M., Fraser P., St. George-Hyslop P., Van Leuven F. Phosphorylation, subcellular localization and membrane orientation of the Alzheimer disease associated presenilins. J. Biol. Chem. 272:1997;3590-3598.
17. DeStrooper B., Saftig P., Craessaerts K., Vanderstichele H., Guhde G., Annaert W., Von Figura K., Van Leuven F. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature. 391:1998;387-390.
18. Doan A., Thinakaran G., Borchelt D. R., Slunt H. H., Ratovitsky T., Podlisny M., Selkoe D. J., Seeger M., Gandy S. E., Price D. L., Sisodia S. S. Protein topology of preseniin-1. Neuron. 17:1996;1023-1030.
19. Dominguez M., Dejgaard K., Fuellerkrug J., Dahan S., Fazel A., Paccaud J. P., Thomas D. Y., Bergeron J. J. M., Nilsson T. gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COP I and II coatomer. J. Cell Biol. 140:1998;751-765.
20. Duff K., Eckman C., Zehr C., Yu X., Prada C.-M., Perez-Tur J., Hutton M., Buee L., Harigaya Y., Yager D., Morgan D., Gordon M. N., Holcomb L., Refolo L., Zenk B., Hardy J., Younkin S. Increased amyloid-β42(43) in brains of mice expressing mutant presenilin 1. Nature. 383:1996;710-713.
21. Elder G. A., Tezapsidis N., Carter J., Shioi J., Bouras C., Li H.-C., Johnston J. M., Efthimiopoulos S., Friedrich V. L., Robakis N. K. Identification and neuron-specific expression of the S182/presenilin I protein in human and rodent brains. J. Neurosci. Res. 45:1996;308-320.
22. 2+ and cAMP. Pflugers Arch.-Eur. J. Physiol. 430:1995;374-380.
23. Gonatas J. O., Mezitis S. G., Stieber A., Fleischer S., Gonatas N. K. MG-160. A novel sialoglycoprotein of the medial cisternae of the Golgi apparatus. J. Biol. Chem. 264:1989;646-653.
24. Hobman T. C., Zhao B., Chan H., Farquhar M. G. Immunoisolation and characterization of a subdomain of the endoplasmic reticulum that concentrates proteins involved in COPII vesicle biogenesis. Mol. Biol. Cell. 9:1998;1265-1278.
25. Holcomb L., Gordon M. N., McGowan E., Yu X., Benkovic S., Jantzen P., Wright K., Saad I., Mueller R., Morgan D., Sanders S., Zehr C., O'Campo K., Hardy J., Prada C. M., Eckman C., Younkin S., Hsiao K., Duff K. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med. 4:1998;97-100.
26. Huovila A. J., Eder A. M., Fuller S. D. Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment. J. Cell Biol. 118:1992;1305-1320.
27. Itin C., Shindler R., Hauri H. P. Targeting of protein ERGIC-53 to the ER/ERGIC/cis-Golgi recycling pathway. J. Cell Biol. 131:1995;57-67.
28. Johnston J. A., Ward C. L., Kopito R. R. Aggresomes: A cellular response to misfolded proteins. J. Cell Biol. 143:1998;1883-1898.
29. Kim T. W., Pettingell W. H., Hallmark O. G., Moir R. D., Wasco W., Tanzi R. E. Endoproteolytic cleavage and proteosomal degradation of presenilin 2 in transfected cells. J. Biol. Chem. 272:1997;11006-11010.
30. Kovacs D., Faucett H., Page K., Kim T.-W., Moir R., Merriam D., Hollister R., Hallmark O., Mancini R., Felsenstein K., Hyman B., Tanzi R., Wasco W. Alzheimer-associated presenilins 1 and 2: Neuronal expression in brain and localization to intracellular membranes in mammalian cells. Nat. Med. 2:1996;224-229.
31. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
32. Lah J. J., Heilman C. J., Nash N. R., Rees H. D., Yi H., Counts S. E., Levey A. I. Light and electron microscopic localization of presenilin-1 in primate brain. J. Neurosci. 17:1997;1971-1980.
33. Lee M. K., Borchelt D. R., Kim G., Thinakaran G., Slunt H. H., Ratovitski T., Martin L. J., Kittur A., Gandy S., Levey A. I., Jenkins N., Copeland N., Price D. L., Sisodia S. S. Hyperaccumulation of FAD-linked presenilin 1 variants in vivo. Nat. Med. 3:1997;756-760.
34. Lee M. K., Slunt H. H., Martin L. J., Thinakaran G., Kim G., Gandy S. E., Seeger M., Koo E., Price D. L., Sisodia S. S. Expression of presenilin 1 and 2 (PS1 and PS2) in human and murine tissues. J. Neurosci. 16:1996;7513-7525.
35. Levitan D., Doyle T. G., Brousseau D., Lee M. K., Thinakaran G., Slunt H. H., Sisodia S. S., Greenwald I. Assessment of normal and mutant human presenilin function in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 93:1996;14940-14944.
36. Levy-Lahad E., Wasco W., Poorkaj P., Romano D. M., Oshima J., Pettingell W. H., Yu C.-E., Jondro P. D., Schmidt S. D., Wang K., Crowley A. C., Fu Y.-H., Guenette S. Y., Galas D., Nemens E., Wijsman E. M., Bird T. D., Schellenberg G. D., Tanzi R. E. Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science. 269:1995;973-977.
37. Li X., Greenwald I. Membrane topology of the C. elegans SEL-12 presenilin. Neuron. 17:1996;1015-1021.
38. Li X., Greenwald I. Additional evidence for an eight-transmembrane-domain topology for Caenorhabditis elegans and human presenilins. Proc. Natl. Acad. Sci. USA. 95:1998;7109-7114.
39. Luzio J. P., Brake B., Banting G., Howell K. E., Braghetta P., Stanley K. K. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem. J. 270:1990;97-102.
40. Moussaoui S., Czech C., Pradier L., Blanchard V., Bonici B., Gohin M., Imperato A., Revah F. Immunohistochemical analysis of presenilin-1 expression in the mouse brain. FEBS Lett. 383:1996;219-222.
41. Naruse S., Thinakaran G., Luo J. J., Kusiak J. W., Tomita T., Iwatsubo T., Qian X., Ginty D. D., Price D. L., Borchelt D. R., Wong P. C., Sisodia S. S. Effects of PS1 deficiency on membrane protein trafficking in neurons. Neuron. 21:1998;1213-1221.
42. Noble L. J., Kalinyak J. E., Pitts L. H., Hall J. J. Fluid-phase endocytosis of horseradish peroxidase by cerebral endothelial cells in primary culture: characterization and kinetic analysis. J. Neurosci. Res. 38:1994;654-663.
43. Paccaud J. P., Reith W., Carpentier J. L., Ravazzola M., Amherdt M., Schekman R., Orci L. Cloning and functional characterization of mammalian homologues of the COPII component Sec23. Mol. Biol. Cell. 7:1996;1535-1546.
44. Perez-Tur J., Froelich S., Prihar G., Crook R., Baker M., Duff K., Wragg M., Busfield F., Lendon C., Clark R. F., Roques P., Fuldner R. A., Johnston J., Cowburn R., Forsell C., Axelman K., Lilius L., Houlden H., Karran E., Roberts G. W., Rossor M., Adams M. D., Hardy J., Goate A., Lannfelt L., Hutton M. A mutation in Alzheimer's disease destroying a splice acceptor site in the presenilin-1 gene. Neuroreport. 7:1995;297-301.
45. Podlisny M. B., Citron M., Amarante P., Sherrington R., Xia W., Zhang J., Diehl T., Levesque G., Fraser P., Haass C., Koo E. H. M., Seubert P., St. George-Hyslop P., Teplow D. B., Selkoe D. J. 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. 3:1997;325-337.
46. Ratovitski T., Slunt H. H., Thinakaran G., Price D. L., Sisodia S. S., Borchelt D. R. Endoproteolytic processing and stabilization of wild-type and mutant presenilin. J. Biol. Chem. 272:1997;24536-24541.
47. Rogaev E. I., Sherrington R., Rogaeva E. A., Levesque G., Ikeda M., Liang Y., Chi H., Lin C., Holman K., Tsuda T., Mar L., Sorbi S., Nacmias B., Piacentini S., Amaducci L., Chumakov I., Cohen D., Lannfelt L., Fraser P. E., Rommens J. M., St. George-Hyslop P. H. 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. 376:1995;775-778.
48. Roth J., Wang Y., Eckhardt A. E., Hill R. L. Subcellular localization of the UDP-N-acetyl-D-galactosamine:Polypeptide N-acetylgalactosaminyltransferase-mediated O-glycosylation reaction in the submaxillary gland. Proc. Natl. Acad. Sci. USA. 91:1994;8935-8939.
49. Schweizer A., Fransen J. A. M., Bachi T., Ginsel L., Hauri H. P. Identification, by a monoclonal antibody of a 53-kDa protein associated with a tubulovesicular compartment at the cis-side of the Golgi apparatus. J. Cell Biol. 107:1988;1643-1653.
50. Seeger M., Nordstedt C., Petanceska S., Kovacs D. M., Gouras G. K., Hahne S., Fraser P., Levesque L., Czernik A. J., St. George-Hyslop P., Sisodia S. S., Thinakaran G., Tanzi R. E., Greengard P., Gandy S. Evidence for phosphorylation and oligomeric assembly of presenilin 1. Proc. Natl. Acad. Sci. USA. 94:1997;5090-5094.
51. Shapiro J., Sciaky N., Lee J., Bosshart H., Angeletti R. H., Bonifacino J. S. Localization of endogenous furin in cultured cell lines. J. Histochem. Cytochem. 45:1997;3-12.
52. Sherrington R., Rogaev E. I., Liang Y., Rogaeva E. A., Levesque G., Ikeda M., Chi H., Li G., Holman K., Tsuda T., Mar L., Foncin J.-F., Bruni A. C., Montesi M. P., Sorbi S., Rainero I., Pinessi L., Nee L., Chumakov I., Pollen D., Brookes A., Sanseau P., Polinsky R. J., Wasco W., DaSilva H. A., Haines J. L., Pericak-Vance M. A., Tanzi R. E., Roses A. D., Fraser P. E., Rommens J. M., St. George-Hyslop P. H. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature. 375:1995;754-760.
53. Sitia R., Meldolesi J. Endoplasmic reticulum: A dynamic patchwork of specialized subregions. Mol. Biol. Cell. 3:1992;1067-1072.
54. Steinman R. M., Brodie S. E., Cohn Z. A. Membrane flow during pinocytosis. J. Cell. Biol. 68:1976;665-687.
55. Storrie B., Madden E. Isolation of subcellular organelles. Methods Enzymol. 182:1990;203-225.
56. Subramaniam V. N., Loh E., Hong W. N-ethylmaleimide-sensitive factor (NSF) and α-soluble NSF attachment proteins (SNAP) mediate dissociation of GS28-syntaxin 5 Golgi SNAP receptors (SNARE) complex. J. Biol. Chem. 272:1997;25441-25444.
57. Subramaniam V. N., Peter F., Philp R., Wong S. H., Hong W. GS28, a 28-kilodalton Golgi SNARE that participates in ER-Golgi transport. Science. 272:1996;1161-1163.
58. Tang B. L., Peter F., Krijnse-Locker J., Low S. H., Griffiths G., Hong W. The mammalian homolog of yeast Sec13p is enriched in the intermediate compartment and is essential for protein transport from the endoplasmic reticulum to the Golgi apparatus. Mol. Cell Biol. 17:1997;256-266.
59. Thinakaran G., Borchelt D. R., Lee M. K., Slunt H. H., Spitzer L., Kim G., Ratovitsky T., Davenport F., Nordstedt C., Seeger M., Hardy J., Levey A. I., Gandy S. E., Jenkins N. A., Copeland N. G., Price D. L., Sisodia S. S. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron. 17:1996b;181-190.
60. Thinakaran G., Harris C. L., Ratovitsky T., Davenport F., Slunt H. H., Price D. L., Borchelt D. R., Sisodia S. S. Evidence that levels of Presenilins(PS1 and PS2) are coordinately regulated by competition for limiting cellular factors. J. Biol. Chem. 272:1997;28415-28422.
61. Thinakaran G., Regard J. B., Bouton C. M. L., Harris C. L., Price D. L., Borchelt D. R., Sisodia S. S. Stable association of presenilin derivatives and absence of presenilin interactions with APP. Neurobiol. Dis. 4:1998;438-453.
62. Thinakaran G., Teplow D. B., Siman R., Greenberg B., Sisodia S. S. Metabolism of the "Swedish" amyloid precursor protein variant in neuro2a (N2a) cells. Evidence that cleavage at the "beta-secretase" site occurs in the Golgi apparatus. J. Biol. Chem. 271:1996a;9390-9397.
63. Walter J., Capell A., Grunberg J., Pesold B., Schindzielorz A., Prior R., Podlisny M. B., Fraser P., St. George Hyslop P., Selkoe D. J., Haass C. The Alzheimer's disease associated presenilins are differentially phosphorylated proteins located predominantly within the endoplasmic reticulum. Mol. Med. 2:1996;673-691.
64. Weisz O. A., Swift A. M., Machamer C. E. Oligomerization of a membrane protein correlates with its retention in the Golgi complex. J. Cell Biol. 122:1993;1185-1196.
65. Yang M., Ellenberg J., Bonicacino J. S., Weissman A. M. The transmembrane domain of a carboxyl-terminal anchored protein determines localization to the endoplasmic reticulum. J. Biol. Chem. 272:1997;1970-1975.
66. Yu G., Chen F., Levesque G., Nishimura M., Zhang D. M., Levesque L., Rogaeva E., Xu D., Liang Y., Duthie M., St. George-Hyslop P. H., Fraser P. E. The presenilin 1 protein is a component of a high molecular weight intracellular complex that contains β-catenin. J. Biol. Chem. 273:1998;16470-16475.
67. Zhang J., Kang D. E., Xia W., Okochi M., Mori H., Selkoe D. J., Koo E. H. Subcellular distribution and turnover of presenilins in transfected cells. J. Biol. Chem. 273:1998;12436-12442.