Localization of presenilin-nicastrin complexes and γ-secretase activity to the trans-Golgi network

Journal of Neurochemistry

Volumn 84, Issue 5, 2003, Pages 1143-1153

  Siman, Robert ^a   Velji, Jamel ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alzheimer's disease; Amyloid; Aspartic protease; Presenilin; trans Golgi network

Indexed keywords

AMYLOID BETA PROTEIN; GAMMA SECRETASE; GLYCOSIDASE; NICASTRIN; PRESENILIN 1; PRESENILIN 2;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL MEMBRANE; CONTROLLED STUDY; DENSITY GRADIENT; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; SIALYLATION; TRANS GOLGI NETWORK;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ENDOPEPTIDASES; CELL COMPARTMENTATION; CELLS, CULTURED; ENDOPEPTIDASES; ENZYME ACTIVATION; FIBROBLASTS; GLYCOSYLATION; MACROMOLECULAR SUBSTANCES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; PRESENILIN-1; PRESENILIN-2; PROTEIN TRANSPORT; STEM CELLS; SUBCELLULAR FRACTIONS; TRANS-GOLGI NETWORK;

ANIMALIA;

EID: 0037339735     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01616.x     Document Type: Article

References (67)

1. Baek S. H., Ohgi K. A., Rose D. W., Koo E. H. Glass C. K. and Rosenfeld M. G. (2002) Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and β-amyloid precursor protein. Cell 110, 55-67.
2. Cao X. and Sudhof T. C. (2001) A transcriptionally active complex of APP with Fe65 and histone acetyltrasferase Tip60. Science 293, 115-120.
3. Chung H. M. and Struhl G. (2001) Nicastrin is required for Presenilin-mediated transmembrane cleavage in Drosophila. Nat. Cell Biol. 3, 1129-1132.
4. 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. and Selkoe D. J. (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid β-protein in both transfected cells and transgenic mice. Nat. Med. 3, 67-72.
5. Cruts M. and Van Broeckhoven C. (1998) Presenilin mutations in Alzheimer's disease. Hum. Mutat 11, 183-190.
6. Cupers P., Bentahir M., Craessaerts K., Orlans I., Vanderstichele H., Saftig P., De Strooper B. and Annaert W. (2001) The discrepancy between presenilin subcellular localization and gamma-secretase processing of amyloid precursor protein. J. Cell Biol. 154, 731-740.
7. De Strooper B., Beullens M., Contreras B., Levesque L., Craessaerts K., Cordell B., Moechars D., Bollen M., Fraser P., George-Hyslop P. S. and Van Leuven F. (1997) Phosphorylation, subcellular localization, and membrane orientation of the Alzheimer's disease-associated presenilins. J. Biol. Chem. 272, 3590-3598.
8. De Strooper B., Saftig P., Craessaerts K., Vanderstichele H., Guhde G., Annaert W., Von Figura K. and Van Leuven F. (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387-390.
9. 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. and Kopan R. (1999) A presenilin-1-dependent γ-secretase-like protease mediates release of Notch intracellular domain. Nature 398, 518-522.
10. Edbauer D., Winkler E., Haass C. and Steiner H. (2002) Presenilin and nicastrin regulate each other and determine amyloid β-peptide production via complex formation. Proc. Natl Acad. Sci. USA 99, 8666-8671.
11. Esler W. P., Kimberly W. T., Ostaszewski B. L. YeW., Diehl T. S., Selkoe D. J. and 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. Francis R., McGrath G., Zhang J., Ruddy D. A., Sym M., Apfeld J., Nicoll, M., Maxwell M., Hai B., Ellis M., C., Parks A. L., Xu W., Li J., Gurney M., Myers R. L., Himes C. S., Hiebsch R., Ruble C., Nye J. S. and Curtis D. (2002) Aph-1 and pen-2 are required for Notch pathway signaling, γ-secretase cleavage of β-APP, and presenilin protein accumulation. Dev. Cell 3, 85-97.
13. Golde T. E., Eckman C. B. and Younkin S. G. (2000) Biochemical detection of Aβ isoforms: implications for pathogenesis, diagnosis, and treatment of Alzheimer's' disease. Biochim. Biophys. Acta 1502, 172-187.
14. Goutte C., Tsunozaki M., Hale V. A. and 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.
15. Greenfield J. P., Tsai J., Gouras G. K., Hai B., Thinakaran G., Checler F., Sisodia S. S., Greengard P. and Xu H. (1999) Endoplasmic reticulum and trans-Golgi network generate distinct populations of Alzheimer β-amyloid peptides. Proc. Natl Acad. Sci. USA 96, 742-747.
16. Hardy J. and Selkoe D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
17. Herreman A., Hartmann D., Annaert W., Saftig P., Craessaerts K., Semeels L., Umans L., Schrijvers V., Checler F., Vanderstichele H., Baekelandt V., Dressel R., Cupers P., Huylebroeck D., Zwijsen A., Van Leuven F. and De Strooper B. (1999) Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 deficiency. Proc. Natl Acad. Sci. USA 96, 11872-11877.
18. Hu Y., Ye Y. and Fortini M. E. (2002) Nicastrin is required for γ-secretase cleavage of the Drosophila Notch receptor. Dev. Cell 2, 69-78.
19. Huse J. T., Liu K., Pijak D. S., Carlin D., Lee V. M. and Doms R. W. (2002) Beta-secretase processing in the trans-Golgi network preferentially generates truncated amyloid species that accumulate in Alzheimer's disease brain. J. Biol. Chem. 277, 16278-16284.
20. Kaether C., Lammich S., Edbauer D., Ertl M., Rietdorf J., Capell A., Steiner H. and Haass C. (2002) Presenilin-1 affects trafficking and processing of betaAPP and is targeted in a complex with nicastrin to the plasma membrane. J. Cell Biol. 158, 551-561.
21. Kimberly W. T., Xia W., Rahmati T., Wolfe M. S. and Selkoe D. J. (2000) The transmembrane aspartates in presenilin 1 and 2 are obligatory for γ-secretase activity and amyloid β-protein generation. J. Biol. Chem. 275, 3173-3178.
22. Kimberly W. T., Zheng J. B., Guenette S. Y. and Selkoe D. J. (2001) The intracellular domain of the β-amyloid precursor protein is stabilized by Fe65 and translocates to the nucleus in a notch-like manner. J. Biol. Chem. 276, 40288-40292.
23. Kimberly W. T., LaVoie M. J., Ostaszewski B. L., Ye W., Wolfe M. S. and Selkoe D. J. (2002) Complex N-linked glycosylated nicastrin associates with active γ-secretase and undergoes tight cellular regulation. J. Biol. Chem. 277, 35113-35117.
24. Kitazume S., Tachida Y., Oka R., Shirotani K., Saido T. C. and Hashimoto Y. (2001) Alzheimer's beta-secretase, beta-site amyloid precursor protein-cleaving enzyme, is responsible for cleavage secretion of a Golgi-resident sialyltransferase. Proc. Natl. Acad. Sci. USA 98, 13554-13559.
25. Kopan R. and Goate A. (2002) Aph-2/Nicastrin: an essential component of γ-secretase and regulator of Notch signaling and presenilin localization. Neuron 33, 321-324.
26. Kovacs D. M., Fausett H. J., Page K. J., Kim T. W., Moir R. D., Merriam D. E., Hollister R. D., Hallmark O. G., Mancini R., Felsenstein K. M., Hyman B. T., Tanzi R. E. and Wasco W. (1996) Alzheimer-associated presenilins 1 and 2: neuronal expression in brain and localization to intracellular membranes in mammalian cells. Nat. Med. 2, 224-229.
27. Lah J. J. and Levey A. I. (2000) Endogenous presenilin-1 targets to endocytic rather than biosynthetic compartments. Mol. Cell. Neurosci. 16, 111-126.
28. Lee S.-F., Shah S., Li H., Yu C., Han W. and Yu G. (2002) Mammalian Aph-1 interacts with presenilin and nicastrin, and is required for intramembrane proteolysis of APP and Notch. J. Biol. Chem. 277, 45013-45019.
29. Leem J. Y., Vijayan S., Han P., Cai D., Machura M., Lopes K. O., Veselits M. L., Xu H. and Thinakaran G. (2002) Presenilin 1 is required for maturation and cell surface accumulation of incastrin. J. Biol. Chem. 277, 19236-19240.
30. Levitan D. and Greenwald I. (1995) Facilitation of lin-12-mediated signalling by sel-12, a Caenorhabditis elegans S182 Alzheimer's disease gene. Nature 377, 351-354.
31. Levitan D., Yu G., St George Hyslop P. and Goutte C. (2001) APH-2/nicastrin functions in LIN-12/Notch signaling in the Caenorhabditis elegans somatic gonad. Dev. Biol. 240, 654-661.
32. 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. and Gardell S. J. (2000) Photoactivated γ-secretase inhibitors directed to the active site covalently label presenilin 1. Nature 405, 689-694.
33. Locker J. K., Griffiths G., Horzinek M. C. and Rottier P. J. (1992) O-glycosylation of the coronavirus M protein: differential localization of sialyltransferases in N- and O-linked glycosylation. J. Biol. Chem. 267, 14094-14101.
34. Lopez-Schier H. and St Johnston D. (2002) Drosophila nicastrin is essential for the intramembranous cleavage of notch. Dev. Cell 2, 79-89.
35. Marambaud P., Shioi J., Serban G., Georgakopoulos A., Sarner S., Nagy V., Baki L., Wen P., Efthimiopoulos S., Shao Z., Wisniewski T. and Robakis N. K. (2002) A presenilin-1/γ-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J. 21, 1948-1956.
36. Moore C. L., Leatherwood D. D., Diehl T. S., Selkoe D. J. and Wolfe M. S. (2000) Difluoro ketone peptidomimetics suggest a large S1 pocket for Alzheimer's γ-secretase: implications for inhibitor design. J. Med. Chem. 43, 3434-3442.
37. Murayama O., Tomita T., Nihonmatsu N., Murayama M., Sun X., Honda T., Iwatsubo T. and Takashima A. (1999) Enhancement of amyloid β42 secretion by 28 different presenilin 1 mutations of familial Alzheimer's disease. Neurosci. Lett. 265, 61-63.
38. 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. and Sisodia S. S. (1998) Effects of PS1 deficiency on membrane protein trafficking in neurons. Neuron 21, 1213-1221.
39. Ni C. Y., Murphy M. P., Golde T. E. and Carpenter G. (2001) γ-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294, 2179-2181.
40. Paulson J. C. and Colley K. J. (1989) Glycosyltransferases. Structure, localization, and control of cell type-specific glycosylation. J. Biol. Chem. 264, 17615-17618.
41. Petanceska S. S., Seeger M., Checler F. and Gandy S. (2000) Mutant presenilin 1 increases the levels of Alzheimer amyloid beta-peptide Abeta42 in late compartments of the constitutive secretory pathway. J. Neurochem. 74, 1878-1884.
42. Rogaev E. I., Sherrington R., Rogaeva E. A., Levesque G., Ikeda M., Liang Y., Chi H., Lin C., Holamn K., Tsuda T., Mar L., Sorbi S., Nacmias B., Piacenti S., Amaducci L., Chumakov I., Cohen D., Lannfelt L., Fraser P. E., Rommens J. M. and 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.
43. Sastre M. Steiner H., Fuchs K., Capell A., Multhaup G., Condron M. M., Teplow D. B. and Haass C. (2001) Presenilin-dependent γ-secretase processing of β-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Report 2, 835-841.
44. Scheuner D., Eckman C., Jensen M., Song X., Citron M., Suzuki N., Bird T. D., Hardy J., Hutton M., Kukull W., Larson E., Levy-Lahad E., Viitanen M., Peskind E., Poorkaj P., Schellenberg G., Tanzi R., Wasco W., Lannfelt L., Selkoe D. and Younkin S. (1996) Secreted amyloid β-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. 2, 864-870.
45. 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. and Zaczek R. (2000) Presenilin-1 and -2 are molecular targets for γ-secretase inhibitors. J. Biol. Chem. 275, 34086-34091.
46. Selkoe D. J. (1998) The cell biology of β-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell Biol. 8, 447-453.
47. Shearman M. S., Beher D., Clarke E. E., Lewis H. D., Harrison T., Hunt P., Nadin A., Smith A. L., Stevenson G. and Castro J. L. (2000) L-685 458, an aspartyl protease transition state mimic is a potent inhibitor of amyloid beta-protein precursor γ-secretase activity. Biochemistry 39, 8698-8704.
48. Shen J., Bronson R. T., Chen D. F., Xia W., Selkoe D. J. and Tonegawa S. (1997) Skeletal and CNS defects in presenilin-1-deficient mice. Cell 89, 629-639.
49. Sisodia S. S. and St George-Hyslop P. H. (2002) γ-Secretase, Notch, Abeta and Alzheimer's disease: where do the presenilins fit in? Nat. Rev. Neurosci. 3, 281-290.
50. Steiner H., Capell A., Pesold B., Citron M., Kloetzel P. M., Selkoe D. J., Romig H., Mendla K. and Haass C. (1998) Expression of Alzheimer's disease-associated presenilin-1 is controlled by proteolytic degradation and complex formation. J. Biol. Chem. 273, 32322-32331.
51. Steiner H., Winkler, E., Edbauer D., Prokop S., Basset G., Yamasaki A., Kostka M. and Haass C. (2002) Pen-2 is an integral component of the γ-secretase complex required for coordinated expression of presenilin and nicastrin. J. Biol. Chem. 277, 39062-39065.
52. Tang D. G., Tokumoto Y. M., Apperly J. A., Lloyd A. C. and Raff M. C. (2001) Lack of replicative senescence in cultured rat oligodendrocyte precursor cells. Science 291, 868-871.
53. Tanzi R. E., Kovacs D. M., Kim T. W., Moir R. D., Guenette S. Y. and Wasco W. (1996) The gene defects responsible for familial Alzheimer's disease. Neurobiol. Dis. 3, 159-168.
54. 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. and Sisodia S. S. (1996) Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17, 181-190.
55. Tomita T., Watabiki T., Takikawa R., Morohashi Y., Takasugi N., Kopan R., De Strooper B. and Iwatsubo T. (2001) The first proline of PALP motif at the C terminus of presenilins is obligatory for stabilization, complex formation, and γ-secretase activities of presenilins. J. Biol. Chem. 276. 33273-33281.
56. Tomita T., Katayama R., Takikawa R. and Iwatsubo T. (2002) Complex N-glycosylated form of nicastrin is stabilized and selectively bound to presenilin fragments. FEBS Lett. 520, 117-121.
57. Turner A. J. and Hooper N. M. (1999) Role for ADAM-family proteinases as membrane protein secretases. Biochem. Soc. Trans. 27, 255-259.
58. Walter J., Kaether C., Steiner H. and Haass C. (2001) The cell biology of Alzheimer's disease: uncovering the secrets of secretases. Curr. Opin. Neurobiol. 11, 585-590.
59. Weidemann A., Eggert S., Reinhard F. B., Vogel M., Paliga K., Baier G., Masters C. L., Beyreuther K. and Evin G. (2002). A novel ε-cleavage within the transmembrane domain of the Alzheimer amyloid precursor protein demonstrates homology with Notch processing. Biochemistry 41, 2825-2835.
60. Wolfe M. S., Xia W., Ostaszewski B. L., Diehl T. S., Kimberly W. T. and Selkoe D. J. (1999) Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 398, 513-517.
61. Wong P. C., Zheng H., Chen H., Becher M. W., Sirinathsinghji D. J., Trumbauer M. E., Chen H. Y., Price D. L., Van der Ploeg L. H. and Sisodia S. S, (1997) Presenilin 1 is required for Notch1 and DIII expression in the paraxial mesoderm. Nature 387, 288-292.
62. Xia W., Ray W. J., Ostaszewski B. L., Rahmati T., Kimberly W. T., Wolfe M. S., Zhang J., Goate A. M. and Selkoe D. J. (2000) Presenilin complexes with the C-terminal fragments of amyloid precursor protein at the sites of amyloid beta-protein generation. Proc. Natl Acad. Sci USA 97, 9299-9304.
63. Xu H., Sweeney D., Wang R., Thinakaran G., Lo A. C. Y., Sisodia S. S., Greengard P. and Gandy S. (1997) Generation of Alzheimer β-amyloid protein in the trans-Golgi network in the apparent absence of vesicle formation. Proc. Natl Acad. Sci. USA 94, 3748-3752.
64. Yang D. S., Tandon A., Chen F., Yu G., Yu H., Arawaka S., Hasegawa H., Duthie M., Schmidt S. D., Ramabhadran T. V. Nixon R. A., Mathews P. M., Gandy S. E., Mount H. T., St George-Hyslop P. and Fraser P. E. (2002) Mature glycosylation and trafficking of nicastrin modulate its binding to presenilins. J. Biol. Chem. 277, 28135-28142.
65. 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. and St George-Hyslop P. (2000) Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and betaAPP processing. Nature 407, 48-54.
66. Zhang J., Kang D. E., Xia W., Okochi M., Mori H., Selkoe D. J. and Koo E. H. (1998) Subcellular distribution and turnover of presenilins in transfected cells. J. Biol. Chem 273, 12436-12442.
67. Zhang Z., Nadeau P., Song W., Donoviel D., Yuan M., Bemstein A. and 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.