The ubiquitin ligase synoviolin up-regulates amyloid β production by targeting a negative regulator of γ-secretase, Rer1, for degradation

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44203-44211

  Tanabe, Chiaki ^a   Maeda, Tomoji ^a   Zou, Kun ^a   Liu, Junjun ^a   Liu, Shuyu ^a   Nakajima, Toshihiro ^b   Komano, Hiroto ^a  

^a IWATE MEDICAL UNIVERSITY   (Japan)

^b TOKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; AMYLOID PRECURSOR PROTEINS; DOMINANT NEGATIVE; ENDOPLASMIC RETICULUM; GLYCOSYLATED; KNOCKOUT MICE; NEGATIVE REGULATORS; NICASTRIN; OVER-EXPRESSION; PROTEASOMES; PROTEIN RETENTION; SECRETASE COMPLEX; SECRETASES; UBIQUITIN LIGASES;

CELL CULTURE; CELL MEMBRANES; FIBROBLASTS; GLYCOPROTEINS;

PROTEINS;

AMYLOID BETA PROTEIN; GAMMA SECRETASE; MEMBRANE PROTEIN; NICASTRIN; PROTEASOME; RETENTION IN ENDOPLASMIC RETICULUM 1 PROTEIN; SYNOVIOLIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; GENE INACTIVATION; GENE OVEREXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; FIBROBLASTS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; PROTEIN BINDING; PROTEOLYSIS; REPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION;

MUS;

EID: 84871769062     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.365296     Document Type: Article

References (31)

1. 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
2. Kimberly, W. T., LaVoie, M. J., Ostaszewski, B. L., Ye, W., Wolfe, M. S., and Selkoe, D. J. (2003) γ-Secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc. Natl. Acad. Sci. U.S.A. 100, 6382-6387
3. Dries, D. R., and Yu, G. (2008) Assembly, maturation, and trafficking of the gamma-secretase complex in Alzheimer's disease. Curr. Alzheimer Res. 5, 132-146
4. Capell, A., Kaether, C., Edbauer, D., Shirotani, K., Merkl, S., Steiner, H., and Haass, C. (2003) Nicastrin interacts with γ-secretase complex components via the N-terminal part of its transmembrane domain. J. Biol. Chem. 278, 52519-52523
5. Spasic, D., Raemaekers, T., Dillen, K., Declerck, I., Baert, V., Serneels, L., Füllekrug, J., and Annaert, W. (2007) Rer1p competes with APH-1 for binding to nicastrin and regulates γ-secretase complex assembly in the early secretory pathway. J. Cell Biol. 176, 629-640
6. Kaether, C., Scheuermann, J., Fassler, M., Zilow, S., Shirotani, K., Valkova, C., Novak, B., Kacmar, S., Steiner, H., and Haass, C. (2007) Endoplasmic reticulum retention of the γ-secretase complex component Pen2 by Rer1. EMBO Rep. 8, 743-748
7. Shah, S., Lee, S. F., Tabuchi, K., Hao, Y. H., Yu, C., LaPlant, Q., Ball, H., Dann, C. E., 3rd, Südhof, T., and Yu, G. (2005) Nicastrin functions as a γ-secretase-substrate receptor. Cell 122, 435-447
8. 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
9. 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 nicastrin. J. Biol. Chem. 277, 19236-19240
10. 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
11. Amano, T., Yamasaki, S., Yagishita, N., Tsuchimochi, K., Shin, H., Kawahara, K., Aratani, S., Fujita, H., Zhang, L., Ikeda, R., Fujii, R., Miura, N., Komiya, S., Nishioka, K., Maruyama, I., Fukamizu, A., and Nakajima, T. (2003) Synoviolin/Hrd1, an E3 ubiquitin ligase, as a novel pathogenic factor for arthropathy. Genes Dev. 17, 2436-2449
12. Bays, N. W., Gardner, R. G., Seelig, L. P., Joazeiro, C. A., and Hampton, R. Y. (2001) Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 3, 24-29
13. Bordallo, J., Plemper, R. K., Finger, A., and Wolf, D. H. (1998) Der3p/Hrd1p is required for endoplasmic reticulum-associated degradation of misfolded lumenal and integral membrane proteins. Mol. Biol. Cell 9, 209-222
14. Christianson, J. C., Olzmann, J. A., Shaler, T. A., Sowa, M. E., Bennett, E. J., Richter, C. M., Tyler, R. E., Greenblatt, E. J., Harper, J. W., and Kopito, R. R. (2012) Defining human ERAD networks through an integrative mapping strategy. Nat. Cell Biol. 14, 93-105
15. Maeda, T., Marutani, T., Zou, K., Araki, W., Tanabe, C., Yagishita, N., Yamano, Y., Amano, T., Michikawa, M., Nakajima, T., and Komano, H. (2009) An E3 ubiquitin ligase, Synoviolin, is involved in the degradation of immature nicastrin, and regulates the production of amyloid β-protein. FEBS J. 276, 5832-5840
16. Komano, H., Shiraishi, H., Kawamura, Y., Sai, X., Suzuki, R., Serneels, L., Kawaichi, M., Kitamura, T., and Yanagisawa, K. (2002) A new functional screening system for identification of regulators for the generation of amyloid β-protein. J. Biol. Chem. 277, 39627-39633
17. Yagishita, N., Ohneda, K., Amano, T., Yamasaki, S., Sugiura, A., Tsuchimochi, K., Shin, H., Kawahara, K., Ohneda, O., Ohta, T., Tanaka, S., Yamamoto, M., Maruyama, I., Nishioka, K., Fukamizu, A., and Nakajima, T. (2005) Essential role of synoviolin in embryogenesis. J. Biol. Chem. 280, 7909-7916
18. Zou, K., Hosono, T., Nakamura, T., Shiraishi, H., Maeda, T., Komano, H., Yanagisawa, K., and Michikawa, M. (2008) Novel role of presenilins in maturation and transport of integrin β 1. Biochemistry 47, 3370-3378
19. 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 βAPP and is targeted in a complex with nicastrin to the plasma membrane. J. Cell Biol. 158, 551-561
20. Spasic, D., and Annaert, W. (2008) Building γ-secretase: The bits and pieces. J. Cell Sci. 121, 413-420
21. De Strooper, B., and Annaert, W. (2010) Novel research horizons for presenilins and γ-secretases in cell biology and disease. Annu. Rev. Cell Dev. Biol. 26, 235-260
22. Kaneko, M., Ishiguro, M., Niinuma, Y., Uesugi, M., and Nomura, Y. (2002) Human HRD1 protects against ER stress-induced apoptosis through ER-associated degradation. FEBS Lett. 532, 147-152
23. Yamasaki, S., Yagishita, N., Sasaki, T., Nakazawa, M., Kato, Y., Yamadera, T., Bae, E., Toriyama, S., Ikeda, R., Zhang, L., Fujitani, K., Yoo, E., Tsuchimochi, K., Ohta, T., Araya, N., Fujita, H., Aratani, S., Eguchi, K., Komiya, S., Maruyama, I., Higashi, N., Sato, M., Senoo, H., Ochi, T., Yokoyama, S., Amano, T., Kim, J., Gay, S., Fukamizu, A., Nishioka, K., Tanaka, K., and Nakajima, T. (2007) Cytoplasmic destruction of p53 by the endoplasmic reticulum-resident ubiquitin ligase 'Synoviolin'. EMBO J. 26, 113-122
24. Sato, K., Sato, M., and Nakano, A. (2003) Rer1p, a retrieval receptor for ER membrane proteins, recognizes transmembrane domains in multiple modes. Mol. Biol. Cell 14, 3605-3616
25. Schwappach, B. (2008) An overview of trafficking and assembly of neurotransmitter receptors and ion channels (Review). Mol. Membr. Biol. 25, 270-278
26. Valkova, C., Albrizio, M., Röder, I. V., Schwake, M., Betto, R., Rudolf, R., and Kaether, C. (2011) Sorting receptor Rer1 controls surface expression of muscle acetylcholine receptors by ER retention of unassembled α-subunits. Proc. Natl. Acad. Sci. U.S.A. 108, 621-625
27. Sato, K., Sato, M., and Nakano, A. (2001) Rer1p, a retrieval receptor for endoplasmic reticulum membrane proteins, is dynamically localized to the Golgi apparatus by coatomer. J. Cell Biol. 152, 935-944
28. Füllekrug, J., Boehm, J., Röttger, S., Nilsson, T., Mieskes, G., and Schmitt, H. D. (1997) Human Rer1 is localized to the Golgi apparatus and complements the deletion of the homologous Rer1 protein of Saccharomyces cerevisiae. Eur. J. Cell Biol. 74, 31-40
29. Fujita, E., Kouroku, Y., Isoai, A., Kumagai, H., Misutani, A., Matsuda, C., Hayashi, Y. K., and Momoi, T. (2007) Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: Ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II). Hum. Mol. Genet. 16, 618-629
30. Kaminskyy, V., and Zhivotovsky, B. (2012) Proteases in autophagy. Biochim. Biophys. Acta 1824, 44-50
31. Pandey, U. B., Nie, Z., Batlevi, Y., McCray, B. A., Ritson, G. P., Nedlsky, N. B., Schwartz, S. L., DiProspero, N. A., Knight, M. A., Schuldiner, O., Padmanabhan, R., Hild, M., Berry, D. L., Garza, D., Hubbert, C. C., Yao, T. P., Baehrecke, E. H., and Taylor, J. P. (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447, 859-863