Different transmembrane domains associate with distinct endoplasmic reticulum components during membrane integration of a polytopic protein

Molecular Biology of the Cell

Volumn 13, Issue 12, 2002, Pages 4114-4129

  Meacock, Suzanna L ^a,b   Lecomte, Fabienne J L ^a   Crawshaw, Samuel G ^a   High, Stephen ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b EUROPEAN PATENT OFFICE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; OPSIN; POLYTOPIC PROTEIN; UNCLASSIFIED DRUG; CELL RECEPTOR; CHAPERONE; CROSS LINKING REAGENT; ISOPROTEIN; NEUROTENSIN; RECEPTOR; SEC61 PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOGENESIS; ENDOPLASMIC RETICULUM; GENE INSERTION; HUMAN; MEMBRANE STRUCTURE; OBSERVATION; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; ANIMAL; BIOLOGICAL MODEL; CATTLE; CELL MEMBRANE; CHEMISTRY; DOG; GENETIC TRANSCRIPTION; GLYCOSYLATION; METABOLISM; MICROSOME; PANCREAS; PROTEIN BINDING; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; RAT; SERODIAGNOSIS; SITE DIRECTED MUTAGENESIS;

ANIMALS; CATTLE; CELL MEMBRANE; CROSS-LINKING REAGENTS; DOGS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROSOMES; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; NEUROTENSIN; OPSIN; PANCREAS; PRECIPITIN TESTS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, PEPTIDE; TRANSCRIPTION, GENETIC;

EID: 0036906637     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-04-0198     Document Type: Article

References (35)

1. Adamus, G., Zam, Z.S., Arendt, A., Palczewski, K., McDowell, J.H., and Hargrave, P.A. (1991). Anti-rhodopsin monoclonal antibodies of defined specificity: characterization and application. Vision Res. 31, 17-31.
2. Beckmann, R., Spahn, C.M., Eswar, N., Helmers, J., Penczek, P.A., Sali, A., Frank, J., and Blobel, G. (2001). Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372.
3. Blobel, G., and Dobborstein, B. (1975). Transfer of proteins across membranes 1. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67, 835-851.
4. Borel, A.C., and Simon, S.M. (1996a). Biogenesis of polytopic membrane proteins: Membrane segments assemble within translocation channels prior to membrane assembly. Cell 85, 379-389.
5. Borel, A.C., and Simon, S.M. (1996b). Biogenesis of polytopic membrane proteins: Membrane segments of P-glycoprotein sequentially translocate to span the ER membrane. Biochemistry 35, 10587-10594.
6. Colley, N.J., Baker, E.K., Stamnes, M.A., and Zuker, C.S. (1991). The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67, 255-263.
7. Denzer, A.J., Nabholtz, C.E., and Spiess, M. (1995). Transmembrane orientation of signal-anchor proteins is affected by the folding state but not the size of the N-terminal domain. EMBO J. 14, 6311-6317.
8. Do, H., Falcone, D., Lin, J., Andrews, D.W., and Johnson, A.E. (1996). The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell 85, 369-378.
9. Haigh, N.G., and Johnson, A.E. (2002). A new role for BiP: Closing the aqueous translocon pore during protein integration into the ER membrane. J. Cell Biol. 156, 261-270.
10. Hartmann, E., Sommer, T., Prehn, S., Gorlich, D., Jentsch, S., and Rapoport, T.A. (1994). Evolutionary conservation of components of the protein translocation complex. Nature 367, 654-657.
11. Hegde, R.S., and Lingappa, V.R. (1996). Sequence-specific alteration of the ribosome-membrane junction exposes nascent secretory proteins to the cytosol. Cell 85, 217-228.
12. Heinrich, S.U., Mothes, W., Brunner, J., and Rapoport, T.A. (2000). The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell 102, 233-244.
13. Heymann, J.A., and Subramaniam, S. (1997). Expression, stability, and membrane integration of truncation mutants of bovine rhodopsin. Proc. Natl. Acad. Sci. USA 94, 4966-4971.
14. High, S., and Laird, V. (1997). Membrane protein biosynthesis - All sewn up? Trends Cell Biol. 7, 206-210.
15. High, S., Laird, V., and Oliver, J.D. (1997). The Biosynthesis of Membrane Proteins at the Endoplasmic Reticulum, Austin, TX: R.G. Landes Co.
16. High, S., et al. (1993). Site-specific photocross-linking reveals that Sec61p and TRAM contact different regions of a membrane inserted signal sequence. J. Biol. Chem. 268, 26745-26751.
17. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and Pease, L.R. (1989). Engineering hybrid genes without the use of restriction enzymes: Gene splicing by overlap extension. Gene 77, 61-68.
18. 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.
19. Keenan, R.J., Freymann, D.M., Stroud, R.M., and Walter, P. (2001). The signal recognition particle. Annu. Rev. Biochem. 70, 755-775.
20. Kuroiwa, T., Sakaguchi, M., Mihara, K., and Omura, T. (1993). Detection of a novel 9-kDa endoplasmic reticulum membrane protein in mammalian cells by chemical cross-linking with translocating nascent peptides. J. Biochem. 114, 541-546.
21. Laird, V., and High, S. (1997). Discrete cross-linking products identified during membrane protein biosynthesis. J. Biol. Chem. 272, 1983-1989.
22. Liao, S., Lin, J., Do, H., and Johnson, A.E. (1997). Both lumenal and cytosolic gating of the aqueous ER translocon pore are regulated from inside the ribosome during membrane protein integration. Cell 90, 31-41.
23. Martoglio, B., and Dobberstein, B. (1996). Snapshots of membrane-translocating proteins. Trends Cell Biol. 6, 142-147.
24. Matlack, K.E., Mothes, W., and Rapoport, T.A. (1998). Protein translocation: Tunnel vision. Cell 92, 381-390.
25. Menetret, J.F., Neuhof, A., Morgan, D.G., Plath, K., Radermacher, M., Rapoport, T.A., and Akey, C.W. (2000). The structure of ribosome-channel complexes engaged in protein translocation. Mol. Cell 6, 1219-1232.
26. Menon, S.T., Han, M., and Sakmar, T.P. (2001). Rhodopsin: Structural basis of molecular physiology. Physiol. Rev. 81, 1659-1688.
27. Miller, J.D., Tajima, S., Lauffer, L., and Walter, P. (1995). The β subunit of the signal recognition particle receptor is a transmembrane GTPase that anchors the α subunit, a peripheral membrane GTPase, to the endoplasmic reticulum membrane. J. Cell Biol. 128, 273-282.
28. Mothes, W., Heinrich, S.U., Graf, R., Nilsson, I., von Heijne, G., Brunner, J., and Rapoport, T.A. (1997). Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell 89, 523-533.
29. Mothes, W., Prehn, S., and Rapoport, T.A. (1994). Systematic probing of the environment of a translocating secretory protein during translocation through the ER membrane. EMBO J. 13, 3973-3982.
30. Nicchitta, C.V., and Blobel, G. (1993). Lumenal proteins of the mammalian endoplasmic reticulum are required to complete protein translocation Cell 79, 989-998.
31. Paver, J.L., Hawkins, H.C., and Freedman, R.B. (1989). Preparation and characterization of dog pancreas microsomal membranes specifically depleted of protein disulphide-isomerase. Biochem. J. 257, 657-663.
32. Schröder, K., Martoglio, B., Hofmann, M., Holscher, C., Hartmann, E., Prehn, S., Rapoport, T.A., and Dobberstein, B. (1999). Control of glycosylation of MHC class II-associated invariant chain by translocon-associated RAMP4. EMBO J. 18, 4804-4815.
33. Tucker, J., and Grisshammer, R. (1996). Purification of a rat neurotensin receptor expressed in Escherichia coli. Biochem. J. 317, 891-899.
34. 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.
35. Wolin, S.L., and Walter, P. (1988). Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J. 7, 3559-3569.