A misassembled transmembrane domain of a polytopic protein associates with signal peptide peptidase

Biochemical Journal

Volumn 384, Issue 1, 2004, Pages 9-17

  Crawshaw, Samuel G ^a   Martoglio, Bruno ^b   Meacock, Suzanna L ^a,c   High, Stephen ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ETH ZURICH   (Switzerland)

^c EUROPEAN PATENT OFFICE   (Germany)

Author keywords

Endoplasmic reticulum; Membrane protein; Opsin; Quality control; Signal peptide peptidase (SPP)

Indexed keywords

BIOLOGICAL MEMBRANES; CROSS CONNECTIONS (WATER DISTRIBUTION); POLYPEPTIDES; QUALITY CONTROL;

ENDOPLASMIC RETICULUM (ER); POLYTOPIC PROTEIN ASSOCIATES; SIGNAL PEPTIDE PEPTIDASE (SPP);

PROTEINS;

MEMBRANE PROTEIN; OPSIN; PEPTIDE FRAGMENT; PROTEIN SUBUNIT; SEC61 PROTEIN; SIGNAL PEPTIDASE; UNCLASSIFIED DRUG;

ARTICLE; ENDOPLASMIC RETICULUM; ENZYME BINDING; MOLECULAR PROBE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; QUALITY CONTROL;

ALTERNATIVE SPLICING; ANIMALS; ASPARTIC ENDOPEPTIDASES; CATTLE; CROSS-LINKING REAGENTS; DIPEPTIDES; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MOLECULAR PROBES; OPSIN; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY;

EID: 9444239782     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041216     Document Type: Article

References (35)

1. Johnson, A. E. and van Waes, M. A. (1999) The translocon: a dynamic gateway at the ER membrane. Annu. Rev. Cell Dev. Biol. 15, 799-842
2. Ellgaard, L. and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191
3. Tsai, B., Ye, Y. and Rapoport, T. A. (2002) Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol. 3, 246-255
4. Lilley, B. N. and Ploegh, H. L. (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature (London) 429, 834-840
5. Ye, Y., Shibata, Y., Yun, C., Ron, D. and Rapoport, T. A. (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature (London) 429, 841-847
6. Ye, Y., Meyer, H. H. and Rapoport, T. A. (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature (London) 414, 652-656
7. Wiertz, E. J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T. R., Rapoport, T. A. and Ploegh, H. L. (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature (London) 384, 432-438
8. High, S., Lecomte, F. J., Russell, S. J., Abell, B. M. and Oliver, J. D. (2000) Glycoprotein folding in the endoplasmic reticulum: a tale of three chaperones? FEBS Lett. 476, 38-41
9. Römisch, K. (1999) Surfing the Sec61 channel: bidirectional protein translocation across the ER membrane. J. Cell. Sci. 112, 4185-4191
10. Beguin, P., Hasler, U., Staub, O. and Geering, K. (2000) Endoplasmic reticulum quality control of oligomeric membrane proteins: topogenic determinants involved in the degradation of the unassembled Na,K-ATPase α subunit and in its stabilization by β subunit assembly. Mol. Biol. Cell 11, 1657-1672
11. Fayadat, L. and Kopito, R. R. (2003) Recognition of a single transmembrane degron by sequential quality control checkpoints. Mol. Biol. Cell 14, 1268-1278
12. Menon, S. T., Man, M. and Sakmar, T. P. (2001) Rhodopsin: structural basis of molecular physiology. Physiol. Rev. 81, 1659-1688.
13. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M. and Miyano, M. (2000) Crystal structure of rhodopsin: A G-protein-coupled receptor. Science (Washington, D.C.) 289, 739-745
14. Hargrave, P. A., McDowell, J. H., Curtis, D. R., Wang, J. K., Juszczak, E., Fong, S. L., Rao, J. K. and Argos, P (1983) The structure of bovine rhodopsin. Biophys. Struct. Mech. 9, 235-244
15. Rattner, A., Sun, H. and Nathans, J. (1999) Molecular genetics of human retinal disease. Annu. Rev. Genet. 33, 89-131
16. Laird, V. and High, S. (1997) Discrete cross-linking products identified during membrane protein biosynthesis. J. Biol. Chem. 272, 1983-1989
17. Meacock, S. L., Lecomte, F. J., Crawshaw, S. G. and High, S. (2002) Different transmembrane domains associate with distinct endoplasmic reticulum components during membrane integration of a polytopic protein. Mol. Biol. Cell (Cambridge, Mass.) 13, 4114-4129
18. Chapple, J. P., Grayson, C., Hardcastle, A. J., Saliba, R. S., van der Spuy, J. and Cheetham, M. E. (2001) Unfolding retinal dystrophies: a role for molecular chaperones? Trends Mol. Med. 7, 414-421
19. Pind, S., Riordan, J. R. and Williams, D. B. (1994) Participation of the endoplasmic reticulum chaperone calnexin (p88, IP90) in the biogenesis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269, 12784-12788
20. Kopito, R. R. (1999) Biosynthesis and degradation of CFTR. Physiol. Rev. 79, S167-S173
21. Meacham, G. C., Patterson, C., Zhang, W., Younger, J. M. and Cyr, D. M. (2001) The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat. Cell Biol. 3, 100-105
22. Swanton, E., High, S. and Woodman, P. (2003) Role of calnexin in the glycan-independent quality control of proteolipid protein. EMBO J. 22, 2948-2958
23. Weihofen, A., Binns, K., Lemberg, M. K., Ashman, K. and Martoglio, B. (2002) Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science (Washington, D.C.) 296, 2215-2218
24. Weihofen, A., Lemberg, M. K., Ploegh, H. L., Bogyo, M. and Martoglio, B. (2000) Release of signal peptide fragments into the cytosol requires cleavage in the transmembrane region by a protease activity that is specifically blocked by a novel cysteine protease inhibitor. J. Biol. Chem. 275, 30951-30956
25. Adamus, G., Zam, Z. S., Arendt, A., Palczewski, K., McDowell, J. H. and Margrave, P. A. (1991) Anti-rhodopsin monoclonal antibodies of defined specificity: characterization and application. Vision Res. 31, 17-31
26. Gilmore, R., Collins, P., Johnson, J., Kellaris, K. and Rapiejko, P. (1991) in Methods in Cell Biology, vol. 34 (Tartakoff, A. M., ed.), pp. 223-239, Academic Press
27. Wilson, R., Allen, A. J., Oliver, J., Brookman, J. L., High, S. and Bulleid, N. J. (1995) The translocation, folding, assembly and redox-dependent degradation of secretory and membrane proteins in semi-permeabilized mammalian cells. Biochem. J. 307, 679-687
28. Weihofen, A., Lemberg, M. K., Friedmann, E., Rueeger, H., Schmitz, A., Paganetti, P, Rovelli, G. and Martoglio, B. (2003) Targeting presenilin-type aspartic protease signal peptide peptidase with γ-secretase inhibitors. J. Biol. Chem. 278, 16528-16533
29. Nyborg, A. C., Kornilova, A. Y., Jansen, K., Ladd, T. B., Wolfe, M. S. and Golde, T. E. (2004) Signal peptide peptidase forms a homodimer that is labeled by an active site directed γ-secretase inhibitor. J. Biol. Chem. 279, 15153-15160
30. Lemberg, M. K. and Martoglio, B. (2002) Requirements for signal peptide peptidase-catalyzed intramernbrane proteolysis. Mol. Cell 10, 735-744
31. Abell, B. M., Jung, M., Oliver, J. D., Knight, B. C., Tyedmers, J., Zimmermann, R. and High, S. (2003) Tail-anchored and signal-anchored proteins utilize overlapping pathways during membrane insertion. J. Biol. Chem. 278, 5669-5678
32. Tian, G., Ghanekar, S. V., Aharony, D., Shenvi, A. B., Jacobs, R. T., Liu, X. and Greenberg, B. D. (2003) The mechanism of γ-secretase: multiple inhibitor binding sites for transition state analogs and small molecule inhibitors. J. Biol. Chem. 278, 28968-28975
33. McCracken, A. A. and Brodsky, J. L. (2003) Evolving questions and paradigm shifts in endoplasmic-reticulum-assciciated degradation (ERAD). Bioessays 25, 868-877
34. Moliaka, Y. K., Grigorenko, A., Madera, D. and Rogaev, E. I. (2004) Impas 1 possesses endoproteolytic activity against multipass membrane protein substrate cleaving the presenilin 1 holoprotein. FEBS Lett. 557, 185-192
35. Nyborg, A. C., Jansen, K., Ladd, T. B., Fauq, A. and Golde, T. E. (2004) An SPP reporter activity assay based on the cleavage of type II membrane protein substrates provides further evidence for an inverted orientation of the SPP active site relative to presenilin. J. Biol. Chem. 279, 43148-43156