The proteolytic processing of the amyloid precursor protein gene family members APLP-1 and APLP-2 involves α-, β-, γ-, and ε-Like cleavages: Modulation of APLP-1 processing by N-glycosylation

Journal of Biological Chemistry

Volumn 279, Issue 18, 2004, Pages 18146-18156

  Eggert, Simone ^a   Paliga, Krzysztof ^b   Soba, Peter ^a   Evin, Genevieve ^c   Masters, Colin L ^c   Weidemann, Andreas ^a   Beyreuther, Konrad ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; DISEASES; ENZYMES; GENES;

AMYLOID PRECURSOR PROTEIN (APP); DISEASE RESEARCH;

NEUROLOGY;

ALPHA SECRETASE; AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN LIKE PROTEIN 1; AMYLOID PRECURSOR PROTEIN LIKE PROTEIN 2; GAMMA SECRETASE; UNCLASSIFIED DRUG;

ALPHA CHAIN; ALZHEIMER DISEASE; ARTICLE; BETA CHAIN; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENETIC TRANSFECTION; GLYCOSYLATION; HUMAN; HUMAN CELL; MULTIGENE FAMILY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROCESSING;

AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ENDOPEPTIDASES; BINDING SITES; CELL LINE; ENDOPEPTIDASES; GLYCOSYLATION; HUMANS; MULTIGENE FAMILY; NERVE TISSUE PROTEINS; PEPTIDE FRAGMENTS; PROTEASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSFECTION;

EID: 2442592973     PISSN: 00219258     EISSN: None     Source Type: Journal    
DOI: 10.1074/jbc.M311601200     Document Type: Article

References (90)

1. Kang, J., Lemaire, H. G., Unterbeck, A., Salbaum, J. M., Masters, C. L., Grzeschik, K. H., Multhaup, G., Beyreuther, K., and Muller-Hill, B. (1987) Nature 325, 733-736
2. Coulson, E. J., Paliga, K., Beyreuther, K., and Masters, C. L. (2000) Neurochem. Int. 36, 175-184
3. Wasco, W., Bupp, K., Magendantz, M., Gusella, J. F., Tanzi, R. E., and Solomon, F. (1992) Proc. Natl. Acad. Sci. U. S. A. 89, 10758-10762
4. Paliga, K., Peraus, G., Kreger, S., Durrwang, U., Hesse, L., Multhaup, G., Masters, C. L., Beyreuther, K., and Weidemann, A. (1997) Eur. J. Biochem. 250, 354-363
5. Wasco, W., Gurubhagavatula, S., Paradis, M. D., Romano, D. M., Sisodia, S. S., Hyman, B. T., Neve, R. L., and Tanzi, R. E. (1993) Nat. Genet. 5, 95-100
6. Slunt, H. H., Thinakaran, G., Von Koch, C., Lo, A. C., Tanzi, R. E., and Sisodia, S. S. (1994) J. Biol. Chem. 269, 2637-2644
7. Zheng, H., Jiang, M., Trumbauer, M. E., Sirinathsinghji, D. J., Hopkins, R., Smith, D. W., Heavens, R. P., Dawson, G. R., Boyce, S., Conner, M. W., and et al. (1995) Cell 81, 525-531
8. Heber, S., Herms, J., Gajic, V., Hainfellner, J., Aguzzi, A., Rulicke, T., von Kretzschmar, H., von Koch, C., Sisodia, S., Tremml, P., Lipp, H. P., Wolfer, D. P., and Muller, U. (2000) J. Neurosci. 20, 7951-7963
9. von Koch, C. S., Zheng, H., Chen, H., Trumbauer, M., Thinakaran, G., van der Ploeg, L. H., Price, D. L., and Sisodia, S. S. (1997) Neurobiol. Aging 18, 661-669
10. Glenner, G. G., and Wong, C. W. (1984) Biochem. Biophys. Res. Commun. 120, 885-890
11. Masters, C. L., Multhaup, G., Simms, G., Pottgiesser, J., Martins, R. N., and Beyreuther, K. (1985) EMBO J. 4, 2757-2763
12. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S., Mendiaz, E. A., Denis, P., Teplow, D. B., Ross, S., Amarante, P., Loeloff, R., Luo, Y., Fisher, S., Fuller, J., Edenson, S., Lile, J., Jarosinski, M. A., Biere, A. L., Curran, E., Burgess, T., Louis, J. C., Collins, F., Treanor, J., Rogers, G., and Citron, M. (1999) Science 286, 735-741
13. Yan, R., Bienkowski, M. J., Shuck, M. E., Miao, H., Tory, M. C., Pauley, A. M., Brashier, J. R., Stratman, N. C., Mathews, W. R., Buhl, A. E., Carter, D. B., Tomasselli, A. G., Parodi, L. A., Heinrikson, R. L., and Gurney, M. E. (1999) Nature 402, 533-537
14. Sinha, S., Anderson, J. P., Barbour, R., Basi, G. S., Caccavello, R., Davis, D., Doan, M., Dovey, H. F., Frigon, N., Hong, J., Jacobson-Croak, K., Jewett, N., Keim, P., Knops, J., Lieberburg, I., Power, M., Tan, H., Tatsuno, G., Tung, J., Schenk, D., Seubert, P., Suomensaari, S. M., Wang, S., Walker, D., John, V., and et al. (1999) Nature 402, 537-540
15. Hussain, I., Powell, D. J., Howlett, D. R., Chapman, G. A., Gilmour, L., Murdock, P. R., Tew, D. G., Meek, T. D., Chapman, C., Schneider, K., Ratcliffe, S. J., Tattersall, D., Testa, T. T., Southan, C., Ryan, D. M., Simmons, D. L., Walsh, F. S., Dingwall, C., and Christie, G. (2000) Mol. Cell. Neurosci. 16, 609-619
16. Esch, F. S., Keim, P. S., Beattie, E. C., Blacher, R. W., Culwell, A. R., Oltersdorf, T., McClure, D., and Ward, P. J. (1990) Science 248, 1122-1124
17. Wang, R., Meschia, J. F., Cotter, R. J., and Sisodia, S. S. (1991) J. Biol. Chem. 266, 16960-16964
18. Lammich, S., Kojro, E., Postina, R., Gilbert, S., Pfeiffer, R., Jasionowski, M., Haass, C., and Fahrenholz, F. (1999) Proc. Natl. Acad. Sci. U. S. A. 96, 3922-3927
19. Buxbaum, J. D., Liu, K. N., Luo, Y., Slack, J. L., Stocking, K. L., Peschon, J. J., Johnson, R. S., Castner, B. J., Cerretti, D. P., and Black, R. A. (1998) J. Biol. Chem. 273, 27765-27767
20. Slack, B. E., Ma, L. K., and Seah, C. C. (2001) Biochem. J. 357, 787-794
21. Koike, H., Tomioka, S., Sorimachi, H., Saido, T. C., Maruyama, K., Okuyama, A., Fujisawa-Sehara, A., Ohno, S., Suzuki, K., and Ishiura, S. (1999) Biochem. J. 343, 371-375
22. Simons, M., de Strooper, B., Multhaup, G., Tienari, P. J., Dotti, C. G., and Beyreuther, K. (1996) J. Neurosci. 16, 899-908
23. Weidemann, A., Eggert, S., Reinhard, F. B., Vogel, M., Paliga, K., Baier, G., Masters, C. L., Beyreuther, K., and Evin, G. (2002) Biochemistry 41, 2825-2835
24. Gu, Y., Misonou, H., Sato, T., Dohmae, N., Takio, K., and Ihara, Y. (2001) J. Biol. Chem. 276, 35235-35238
25. Sastre, M., Steiner, H., Fuchs, K., Capell, A., Multhaup, G., Condron, M. M., Teplow, D. B., and Haass, C. (2001) EMBO Rep 2, 835-841
26. Yu, C., Kim, S. H., Ikeuchi, T., Xu, H., Gasparini, L., Wang, R., and Sisodia, S. S. (2001) J. Biol. Chem. 276, 43756-43760
27. Schroeter, E. H., Kisslinger, J. A., and Kopan, R. (1998) Nature 393, 382-386
28. 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) Nature 398, 518-522
29. 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) Nature 407, 48-54
30. 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) Dev. Cell 3, 85-97
31. Goutte, C., Tsunozaki, M., Hale, V. A., and Priess, J. R. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 775-779
32. Steiner, H., Winkler, E., Edbauer, D., Prokop, S., Basset, G., Yamasaki, A., Kostka, M., and Haass, C. (2002) J. Biol. Chem. 277, 39062-39065
33. Wolfe, M. S., Xia, W., Ostaszewski, B. L., Diehl, T. S., Kimberly, W. T., and Selkoe, D. J. (1999) Nature 398, 513-517
34. De Strooper, B., Saftig, P., Craessaerts, K., Vanderstichele, H., Guhde, G., Annaert, W., Von Figura, K., and Van Leuven, F. (1998) Nature 391, 387-390
35. 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) Nature 405, 689-694
36. Kimberly, W. T., Xia, W., Rahmati, T., Wolfe, M. S., and Selkoe, D. J. (2000) J. Biol. Chem. 275, 3173-3178
37. De Strooper, B. (2003) Neuron 38, 9-12
38. Quinn, K. A., Pye, V. J., Dai, Y. P., Chesterman, C. N., and Owensby, D. A. (1999) Exp. Cell Res. 251, 433-441
39. Jarriault, S., Brou, C., Logeat, F., Schroeter, E. H., Kopan, R., and Israel, A. (1995) Nature 377, 355-358
40. Lu, F. M., and Lux, S. E. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 5663-5667
41. Cao, X., and Sudhof, T. C. (2001) Science 293, 115-120
42. Minopoli, G., de Candia, P., Bonetti, A., Faraonio, R., Zambrano, N., and Russo, T. (2001) J. Biol. Chem. 276, 6545-6550
43. Webster, M. T., Groome, N., Francis, P. T., Pearce, B. R., Sherriff, F. E., Thinakaran, G., Felsenstein, K. M., Wasco, W., Tanzi, R. E., and Bowen, D. M. (1995) Biochem. J. 310, 95-99
44. 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) Neuron 21, 1213-1221
45. Weidemann, A., Paliga, K., Durrwang, U., Czech, C., Evin, G., Masters, C. L., and Beyreuther, K. (1997) Nat. Med. 3, 328-332
46. Walsh, D. M., Fadeeva, J. V., LaVoie, M. J., Paliga, K., Eggert, S., Kimberly, W. T., Wasco, W., and Selkoe, D. J. (2003) Biochemistry 42, 6664-6673
47. Grziwa, B., Grimm, M. O., Masters, C. L., Beyreuther, K., Hartmann, T., and Lichtenthaler, S. F. (2003) J. Biol. Chem. 278, 6803-6808
48. Weidemann, A., Konig, G., Bunke, D., Fischer, P., Salbaum, J. M., Masters, C. L., and Beyreuther, K. (1989) Cell 57, 115-126
49. Lyckman, A. W., Confaloni, A. M., Thinakaran, G., Sisodia, S. S., and Moya, K. L. (1998) J. Biol. Chem. 273, 11100-11106
50. Sisodia, S. S. (1992) Proc. Natl. Acad. Sci. U. S. A. 89, 6075-6079
51. 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) Biochemistry 39, 8698-8704
52. Higaki, J., Quon, D., Zhong, Z., and Cordell, B. (1995) Neuron 14, 651-659
53. Mathews, P. M., Jiang, Y., Schmidt, S. D., Grbovic, O. M., Mercken, M., and Nixon, R. A. (2002) J. Biol. Chem. 277, 36415-36424
54. Citron, M., Diehl, T. S., Gordon, G., Biere, A. L., Seubert, P., and Selkoe, D. J. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 13170-13175
55. Parvathy, S., Hussain, I., Karran, E. H., Turner, A. J., and Hooper, N. M. (1998) Biochemistry 37, 1680-1685
56. Arribas, J., Coodly, L., Vollmer, P., Kishimoto, T. K., Rose-John, S., and Massague, J. (1996) J. Biol. Chem. 271, 11376-11382
57. Mohler, K. M., Sleath, P. R., Fitzner, J. N., Cerretti, D. P., Alderson, M., Kerwar, S. S., Torrance, D. S., Otten-Evans, C., Greenstreet, T., Weerawarna, K., Kronheim, S. R., Petersen, M., Gerhart, M., Kozlosky, C. J., March, C. J., and Black, R. A. (1994) Nature 370, 218-220
58. Crowe, P. D., Walter, B. N., Mohler, K. M., Otten-Evans, C., Black, R. A., and Ware, C. F. (1995) J. Exp. Med. 181, 1205-1210
59. Tsubuki, S., Saito, Y., Tomioka, M., Ito, H., and Kawashima, S. (1996) J. Biochem. (Tokyo) 119, 572-576
60. Figueiredo-Pereira, M. E., Berg, K. A., and Wilk, S. (1994) J. Neurochem. 63, 1578-1581
61. Coux, O., Tanaka, K., and Goldberg, A. L. (1996) Annu. Rev. Biochem. 65, 801-847
62. Fenteany, G., Standaert, R. F., Lane, W. S., Choi, S., Corey, E. J., and Schreiber, S. L. (1995) Science 268, 726-731
63. Tanaka, K. (1995) Mol. Biol. Rep. 21, 21-26
64. Hung, A. Y., Haass, C., Nitsch, R. M., Qiu, W. Q., Citron, M., Wurtman, R. J., Growdon, J. H., and Selkoe, D. J. (1993) J. Biol. Chem. 268, 22959-22962
65. Dyrks, T., Monning, U., Beyreuther, K., and Turner, J. (1994) FEBS Lett. 349, 210-214
66. Elbein, A. D. (1987) Methods Enzymol. 138, 661-709
67. Dovey, H. F., John, V., Anderson, J. P., Chen, L. Z., de Saint Andrieu, P., Fang, L. Y., Freedman, S. B., Folmer, B., Goldbach, E., Holsztynska, E. J., Hu, K. L., Johnson-Wood, K. L., Kennedy, S. L., Kholodenko, D., Knops, J. E., Latimer, L. H., Lee, M., Liao, Z., Lieberburg, I. M., Motter, R. N., Mutter, L. C., Nietz, J., Quinn, K. P., Sacchi, K. L., Seubert, P. A., Shopp, G. M., Thorsett, E. D., Tung, J. S., Wu, J., Yang, S., Yin, C. T., Schenk, D. B., May, P. C., Altstiel, L. D., Bender, M. H., Boggs, L. N., Britton, T. C., Clemens, J. C., Czilli, D. L., Dieckman-McGinty, D. K., Droste, J. J., Fuson, K. S., Gitter, B. D., Hyslop, P. A., Johnstone, E. M., Li, W. Y., Little, S. P., Mabry, T. E., Miller, F. D., and Audia, J. E. (2001) J. Neurochem. 76, 173-181
68. Zhong, Z., Higaki, J., Murakami, K., Wang, Y., Catalano, R., Quon, D., and Cordell, B. (1994) J. Biol. Chem. 269, 627-632
69. Sisodia, S. S., Koo, E. H., Beyreuther, K., Unterbeck, A., and Price, D. L. (1990) Science 248, 492-495
70. Sahasrabudhe, S. R., Spruyt, M. A., Muenkel, H. A., Blume, A. J., Vitek, M. P., and Jacobsen, J. S. (1992) J. Biol. Chem. 267, 25602-25608
71. Maruyama, K., Kametani, F., Usami, M., Yamao-Harigaya, W., and Tanaka, K. (1991) Biochem. Biophys. Res. Commun. 179, 1670-1676
72. Parvathy, S., Hussain, I., Karran, E. H., Turner, A. J., and Hooper, N. M. (1998) Biochem. Soc. Trans. 26, 242
73. Turner, R. T., III, Koelsch, G., Hong, L., Castanheira, P., Ermolieff, J., Ghosh, A. K., Tang, J., Castenheira, P., and Ghosh, A. (2001) Biochemistry 40, 10001-10006
74. Citron, M., Teplow, D. B., and Selkoe, D. J. (1995) Neuron 14, 661-670
75. Kitazume, S., Tachida, Y., Oka, R., Shirotani, K., Saido, T. C., and Hashimoto, Y. (2001) Proc. Natl. Acad. Sci. U. S. A. 98, 13554-13559
76. Kitazume, S., Tachida, Y., Oka, R., Kotani, N., Ogawa, K., Suzuki, M., Dohmae, N., Takio, K., Saido, T. C., and Hashimoto, Y. (2003) J. Biol. Chem. 278, 14865-14871
77. Lichtenthaler, S. F., Dominguez, D. I., Westmeyer, G. G., Reiss, K., Haass, C., Saftig, P., De Strooper, B., and Seed, B. (2003) J. Biol. Chem. 278, 48713-48719
78. Haass, C., Schlossmacher, M. G., Hung, A. Y., Vigo-Pelfrey, C., Mellon, A., Ostaszewski, B. L., Lieberburg, I., Koo, E. H., Schenk, D., Teplow, D. B., and Selkoe, D. J. (1992) Nature 359, 322-325
79. Lichtenthaler, S. F., Wang, R., Grimm, H., Uljon, S. N., Masters, C. L., and Beyreuther, K. (1999) Proc. Natl. Acad. Sci. U. S. A. 96, 3053-3058
80. Lichtenthaler, S. F., Beher, D., Grimm, H. S., Wang, R., Shearman, M. S., Masters, C. L., and Beyreuther, K. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 1365-1370
81. Murphy, M. P., Hickman, L. J., Eckman, C. B., Uljon, S. N., Wang, R., and Golde, T. E. (1999) J. Biol. Chem. 274, 11914-11923
82. Tischer, E., and Cordell, B. (1996) J. Biol. Chem. 271, 21914-21919
83. Zhang, J., Ye, W., Wang, R., Wolfe, M. S., Greenberg, B. D., and Selkoe, D. J. (2002) J. Biol. Chem. 277, 15069-15075
84. Weihofen, A., Binns, K., Lemberg, M. K., Ashman, K., and Martoglio, B. (2002) Science 296, 2215-2218
85. Brown, M. S., Ye, J., Rawson, R. B., and Goldstein, J. L. (2000) Cell 100, 391-398
86. Lee, J. R., Urban, S., Garvey, C. F., and Freeman, M. (2001) Cell 107, 161-171
87. Urban, S., Lee, J. R., and Freeman, M. (2002) EMBO J. 21, 4277-4286
88. Sato, T., Dohmae, N., Qi, Y., Kakuda, N., Misonou, H., Mitsumori, R., Maruyama, H., Koo, E. H., Haass, C., Takio, K., Morishima-Kawashima, M., Ishiura, S., and Ihara, Y. (2003) J. Biol. Chem. 278, 24294-24301
89. Scheinfeld, M. H., Ghersi, E., Laky, K., Fowlkes, B. J., and D'Adamio, L. (2002) J. Biol. Chem. 277, 44195-44201
90. May, P., Bock, H. H., Nimpf, J., and Herz, J. (2003) J. Biol. Chem. 277, 18736-18743