A role for presenilin 1 in regulating the delivery of amyloid precursor protein to the cell surface

Neurobiology of Disease

Volumn 11, Issue 1, 2002, Pages 64-82

  Leem, Jae Yoon ^a   Saura, Carlos A ^a,e   Pietrzik, Claus ^b   Christianson, John ^a   Wanamaker, Christian ^a   King, LaShaunda T ^a   Veselits, Margaret L ^a   Tomita, Taisuke ^c   Gasparini, Laura ^d   Iwatsubo, Takeshi ^c   Xu, Huaxi ^d   Green, William N ^a   Koo, Edward H ^b   Thinakaran, Gopal ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d ROCKEFELLER UNIVERSITY   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Acetylcholine receptors; Alzheimer's disease; APP; Nicastrin; PS1; secretase

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ENZYME INHIBITOR; GAMMA SECRETASE; MEMBRANE PROTEIN; NICASTRIN; NICOTINIC RECEPTOR; NOTCH RECEPTOR; PRESENILIN 1;

ARTICLE; BIOTINYLATION; CELL SURFACE; CONTROLLED STUDY; ENZYME INHIBITION; GLYCOSYLATION; HUMAN; HUMAN CELL; INCUBATION TIME; KINETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SIALYLATION;

EID: 0036453087     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1006/nbdi.2002.0546     Document Type: Article

References (56)

1. Annaert, W. G., Esselens, C., Baert, V., Boeve, C., Snellings, G., Cupers, P., Craessaerts, K., & De Strooper, B. (2001) Interaction with telencephalin and the amyloid precursor protein predicts a ring structure for presenilins. Neuron 32, 579-589.
2. Annaert, W. G., Levesque, L., Craessaerts, K., Dterinck, I., Snellings, G., Westaway, D., George-Hyslop, P. S., Cordell, B., Fraser, P., & De Strooper, B. (1999) Presenilin 1 controls gamma-secretase processing of amyloid precursor protein in pre-Golgi compartments of hippocampal neurons. J. Cell Biol. 147, 277-294.
3. Armogida, M., Petit, A., Vincent, B., Scarzello, S., da Costa, C. A., & Checler, F. (2001) Endogenous β-amyloid production in presenilin-deficient embryonic mice fibroblasts. Nat. Cell Biol. 3, 1030-1033.
4. Capell, A., Grunberg, J., Pesold, B., Diehlmann, A., Citron, M., Nixon, R., Beyreuther, K., Selkoe, D. J., & Haass, C. (1998) 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, 3205-3211.
5. Capell, A., Steiner, H., Romig, H., Keck, S., Baader, M., Grim, M. G., Baumeister, R., & Haass, C. (2000) Presenilin-1 differentially facilitates endoproteolysis of the beta-amyloid precursor protein and Notch. Nat. Cell. Biol. 2, 205-211.
6. Caporaso, G. L., Gandy, S. E., Buxbaum, J. D., & Greengard, P. (1992) Chloroquine inhibits intracellular degradation but not secretion of Alzheimer beta/A4 amyloid precursor protein. Proc. Natl. Acad. Sci. USA 89, 2252-2256.
7. De Strooper, B., Annaert, W., Cupers, P., Saftig, P., Craessaerts, K., Mumm, J. S., Schroeter, E. H., Schrijvers, V., Wolfe, M. S., Ray, W. J., Goate, A., & Kopan, R. (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398, 518-522.
8. De Strooper, B., Saftig, P., Craessaerts, K., Vanderstichele, H., Guhde, G., Annaert, W., Von Figura, K., & Van Leuven, F. (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387-390.
9. Eertmoed, A. L., Vallejo, Y. F., & Green, W. N. (1998) Transient expression of heteromeric ion channels. Methods Enzymol. 293, 564-585.
10. Esler, W. P., Kimberly, W. T., Ostaszewski, B. L., Diehl, T. S., Moore, C. L., Tsai, J. Y., Rahmati, T., Xia, W., Selkoe, D. J., & Wolfe, M. S. (2000) Transition-state analogue inhibitors of gamma-secretase bind directly to presenilin-1 Nat. Cell. Biol. 2, 428-434.
11. Esler, W. P., Kimberly, W. T., Ostaszewski, B. L., Ye, W., Diehl, T. S., Selkoe, D. J., & Wolfe, M. S. (2002) Activity-dependent isolation of the presenilin-gamma-secretase complex reveals nicastrin and a gamma substrate. Proc. Natl. Acad. Sci. USA 99, 2720-2725.
12. Gasparini, L., Gouras, G. K., Wang, R., Gross, R. S., Beal, M. F., Greengard, P., & Xu, H. (2001) Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J. Neurosci. 21, 2561-2570.
13. Goutte, C., Tsunozaki, M., Hale, V. A., & Priess, J. R. (2002) APH-1 is a multipass membrane protein essential for the Notch signaling pathway in Caenorhabditis elegans embryos. Proc. Natl. Acad. Sci. USA 99, 775-779.
14. Green, W. N. (1999) Ion channel assembly: Creating structures that function. J. Gen. Physiol. 113, 163-170.
15. Green, W. N., & Wanamaker, C. P. (1998) Formation of the nicotinic acetylcholine receptor binding sites. J. Neurosci. 18, 5555-5564.
16. Harter, C., & Mellman, I. (1992) Transport of the lysosomal membrane glycoprotein lgp120 (lgp-A) to lysosomes does not require appearance on the plasma membrane. J. Cell Biol. 117, 311-325.
17. Kim, S. H., Lah, J. J., Thinakaran, G., Levey, A., & Sisodia, S. S. (2000) Subcellular localization of presenilins: Association with a unique membrane pool in cultured cells. Neurobiol. Dis. 7, 99-117.
18. Kim, S. H., Leem, J. Y., Lah, J. J., Slunt, H. H., Levey, A., Thinakaran, G., & Sisodia, S. S. (2001) Multiple effects of aspartate mutant presenilin 1 on the processing and trafficking of amyloid precursor protein. J. Biol. Chem. 276, 43343-43350.
19. Kimberly, W. T., Xia, W., Rahmati, T., Wolfe, M. S., & Selkoe, D. J. (2000) The transmembrane aspartates in presenilin 1 and 2 are obligatory for gamma-secretase activity and amyloid beta-protein generation. J. Biol. Chem. 275, 3173-3178.
20. Knops, J., Lieberburg, I., & Sinha, S. (1992) Evidence for a nonsecretory, acidic degradation pathway for amyloid precursor protein in 293 cells: Identification of a novel, 22-kDa, beta-peptide-containing intermediate. J. Biol. Chem. 267, 16022-16024.
21. Koo, E. H., & Squazzo, S. L. (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J. Biol. Chem. 269, 17386-17389.
22. Koo, E. H., Squazzo, S. L., Selkoe, D. J., & Koo, C. H. (1996) Trafficking of cell-surface amyloid beta-protein precursor. 1. Secretion, endocytosis and recycling as detected by labeled monoclonal antibody. J. Cell Sci. 109, 991-998.
23. Kopan, R., Schroeter, E. H., Weintraub, H., & Nye, J. S. (1996) Signal transduction by activated mNotch: Importance of proteolytic processing and its regulation by the extracellular domain. Proc. Natl. Acad. Sci. USA 93, 1683-1688.
24. Kuentzel, S. L., Ali, S. M., Altman, R. A., Greenberg, B. D., & Raub, T. J. (1993) The Alzheimer beta-amyloid protein precursor/protease nexin-II is cleaved by secretase in a trans-Golgi secretory compartment in human neuroglioma cells. Biochem. J. 295, 367-378.
25. Kulic, L., Walter, J., Multhaup, G., Teplow, D. B., Baumeister, R., Romig, H., Capell, A., Steiner, H., & Haass, C. (2000) Separation of presenilin function in amyloid beta-peptide generation and endoproteolysis of Notch. Proc. Natl. Acad. Sci. USA 97, 5913-5918.
26. Leem, J. Y., Vijayan, S., Han, P., Cai, D., Machura, M., Lopes, K. O., Veselits, M. L., Xu, H., & Thinakaran, G. (2002) Presenilin 1 is required for maturation and cell surface accumulation of nicastrin. J. Biol. Chem. 277, 19236-19240.
27. Letourneur, F., & Klausner, R. D. (1992) A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69, 1143-1157.
28. 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. (1995) Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269, 973-977.
29. Li, Y. M., Xu, M., Lai, M. T., Huang, Q., Castro, J. L., DiMuzio-Mower, J., Harrison, T., Lellis, C., Nadin, A., Neduvelil, J. G., Register, R. B., Sardana, M. K., Shearman, M. S., Smith, A. L., Shi, X. P., Yin, K. C., Shafer, J. A., & Gardell, S. J. (2000) Photoactivated gamma-secretase inhibitors directed to the active site covalently label presenilin 1. Nature 405, 689-694.
30. Mitra, M., Wanamaker, C. P., & Green, W. N. (2001) Rearrangement of nicotinic receptor alpha subunits during formation of the ligand binding sites. J. Neurosci. 21, 3000-3008.
31. Naruse, S., Thinakaran, G., Luo, J.-J., Kusiak, J. W., Tomiata, T., Iwatsubo, T., Qian, X., Ginty, D. D., Price, D. L., Borchelt, D. R., & Wong, P. C. (1998) Effects of PS1 deficiency on membrane protein trafficking in neurons. Neuron 21, 1213-1221.
32. Petit, A., Bihel, F., da Costa, C. A., Pourquie, O., Checler, F., & Kraus, J. L. (2001) New protease inhibitors prevent gamma-secretase-mediated production of Abeta40/42 without affecting Notch cleavage. Nat. Cell Biol. 3, 507-511.
33. Ratovitski, T., Slunt, H. H., Thinakaran, G., Price, D. L., Sisodia, S. S., & Borchelt, D. R. (1997) Endoproteolytic processing and stabilization of wild-type and mutant presenilin. J. Biol. Chem. 272, 24536-24541.
34. 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. (1995) 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, 775-778.
35. Sadeghi, H., & Birnbaumer, M. (1999) O-glycosylation of the V2 vasopressin receptor. Glycobiology 9, 731-737.
36. Sato, N., Urano, F., Leem, J. Y., Kim, S.-H., Li, M., Donoviel, D., Bernstein, A., Lee, A. S., Ron, D., Veselits, M. L., Sisodia, S. S., & Thinakaran, G. (2000) Upregulation of BiP and CHOP by the unfolded-protein response is independent of presenilin expression. Nat. Cell Biol. 2, 863-870.
37. Seeger, M., Nordstedt, C., Petanceska, S., Kovacs, D. M., Gouras, G. K., Hahne, S., Fraser, P., Levesque, L., Czernik, A. J., George-Hyslop, P. S., Sisodia, S. S., Thinakaran, G., Tanzi, R. E., Greengard, P., & Gandy, S. (1997) Evidence for phosphorylation and oligomeric assembly of presenilin 1. Proc. Natl. Acad. Sci. USA 94, 5090-5094.
38. Seiffert, D., Bradley, J. D., Rominger, C. M., Rominger, D. H., Yang, F., Meredith, J. E. Jr., Wang, Q., Roach, A. H., Thompson, L. A., Spitz, S. M., Higaki, J. N., Prakash, S. R., Combs, A. P., Copeland, R. A., Arneric, S. P., Hartig, P. R., Robertson, D. W., Cordell, B., Stern, A. M., Olson, R. E., & Zaczek, R. (2000) Presenilin-1 and 2 are molecular targets for gamma secretase inhibitors. J. Biol. Chem. 275, 34086-34091.
39. Sherrington, R., Rogaev, E. I., Liang, Y., Rogaeva, E. A., Levesque, G., Ikeda, M., Chi, H., Lin, C., 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., Sansequ, P., Polinsky, R. J., Wasco, W., Da Silva, H. A. R., Haines, J. L., Pericak-Vance, M. A., Tanzi, R. E., Roses, A. D., Fraser, P. E., Rommens, J. M., & St. George-Hyslop, P. H. (1995) Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375, 754-760.
40. Sisodia, S. S., Kim, S. H., & Thinakaran, G. (1999) Function and dysfunction of the presenilins. Am. J. Hum. Genet. 65, 7-12.
41. Skovronsky, D. M., Pijak, D. S., Doms, R. W., & Lee, V. M. (2000) A distinct ER/IC gamma-secretase competes with the proteasome for cleavage of APP. Biochemistry 39, 810-817.
42. Steiner, H., Kostka, M., Romig, H., Basset, G., Pesold, B., Hardy, J., Capell, A., Meyn, L., Grim, M. L., Baumeister, R., Fechteler, K., & Haass, C. (2000) Glycine 384 is required for presenilin-1 function and is conserved in bacterial polytopic aspartyl proteases. Nat. Cell Biol. 2, 848-851.
43. Struhl, G., & Adachi, A. (2000) Requirements for presenilin-dependent cleavage of Notch and other transmembrane proteins. Mol. Cell 6, 625-636.
44. Taniguchi, Y., Karlström, H., Lundkvist, J., Mikzutani, T., Otaka, A., Vestling, M., Bernstein, A., Donoviel, D., Lendhal, U., & Honjo, T. (2002) Notch receptor cleavage depends on but is not directly executed by presenilins. Proc. Natl. Acad. Sci. USA 99, 4014-4019.
45. 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. (1996a) Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17, 181-190.
46. Thinakaran, G., Harris, C. L., Ratovitski, T., Davenport, F., Slunt, H. H., Price, D. L., Borchelt, D. R., & Sisodia, S. S. (1997) Evidence that levels of presenilins (PS1 and PS2) are coordinately regulated by competition for limiting cellular factors. J. Biol. Chem. 272, 28415-28422.
47. Thinakaran, G., Teplow, D. B., Siman, R., Greenberg, B., & Sisodia, S. S. (1996b) Metabolism of the "Swedish" amyloid precursor protein variant in neuro2a (N2a) cells. Evidence that cleavage at the "β-secretase" site occurs in the Golgi apparatus. J. Biol. Chem. 271, 9390-9397.
48. Tollefsen, S. E., & Kornfeld, R. (1983) The B4 lectin from Vicia villosa seeds interacts with N-acetylgalactosamine residues alpha-linked to serine or threonine residues in cell surface glycoproteins. J. Biol. Chem. 258, 5172-5176.
49. Tomita, T., Maruyama, K., Saido, T. C., Kume, H., Shinozaki, K., Tokuhiro, S., Capell, A., Walter, J., Grunberg, J., Haass, C., Iwatsubo, T., & Obata, K. (1997) The presenilin 2 mutation (N1411) 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. USA 94, 2025-2030.
50. Weidemann, A., Konig, G., Bunke, D., Fischer, P., Salbaum, J. M., Masters, C. L., & Beyreuther, K. (1989) Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell 57, 115-126.
51. Weihofen, A., Binns, K., Lemberg, M. K., Ashman, K., & Martoglio, B. (2002) Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 296, 2215-2218.
52. Wiltfang, J., Smirnov, A., Schnierstein, B., Kelemen, G., Matthies, U., Klafki, H. W., Staufenbiel, M., Huther, G., Ruther, E., & Kornhuber, J. (1997) Improved electrophoretic separation and immunoblotting of beta-amyloid (A beta) peptides 1-40, 1-42, and 1-43. Electrophoresis 18, 527-532.
53. Wolfe, M. S., Xia, W., Ostaszewski, B. L., Diehl, T. S., Kimberly, W. T., & Selkoe, D. J. (1999) Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and γ-secretase activity. Nature 398, 513-517.
54. Yu, G., Chen, F., Levesque, G., Nishimura, M., Zhang, D. M., Levesque, L., Rogaeva, E., Xu, D., Liang, Y., Duthie, M., George-Hyslop, P. H. S., & Fraser, P. E. (1998) The presenilin 1 protein is a component of a high molecular weight intracellular complex that contains beta-catenin. J. Biol. Chem. 273, 16470-16475.
55. Yu, G., Nishimura, M., Arawaka, S., Levitan, D., Zhang, L., Tandon, A., Song, Y. Q., Rogaeva, E., Chen, F., Kawarai, T., Supala, A., Levesque, L., Yu, H., Yang, D. S., Holmes, E., Milman, P., Liang, Y., Zhang, D. M., Xu, D. H., Sato, C., Rogaev, E., Smith, M., Janus, C., Zhang, Y., Aebersold, R., Farrer, L. S., Sorbi, S., Bruni, A., Fraser, P., & St George-Hyslop, P. (2000) Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and beta-APP processing. Nature 407, 48-54.
56. Zhang, Z., Nadeau, P., Song, W., Donoviel, D., Yuan, M., Bernstein, A., & Yankner, B. A. (2000) Presenilins are required for gamma-secretase cleavage of beta-APP and transmembrane cleavage of Notch-1. Nat. Cell Biol. 2, 463-465.