Sequential triage of transmembrane segments by Sec61α during biogenesis of a native multispanning membrane protein

Nature Structural and Molecular Biology

Volumn 12, Issue 10, 2005, Pages 870-878

  Sadlish, Heather ^a   Pitonzo, David ^a   Johnson, Arthur E ^b,c   Skach, William R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY SYSTEM   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; AQUAPORIN 4; CARRIER PROTEIN; MEMBRANE PROTEIN; PROTEIN SEC61ALPHA; TRANSLOCON; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; BIOGENESIS; CROSS LINKING; ENDOPLASMIC RETICULUM; LIPID BILAYER; MOLECULAR PROBE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

ANIMALS; AQUAPORIN 4; CELL MEMBRANE; CROSS-LINKING REAGENTS; ENDOPLASMIC RETICULUM; MEMBRANE PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RIBOSOMES;

EID: 27144549973     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb994     Document Type: Article

References (50)

1. Johnson, A. & van Waes, M. The translocon: a dynamic gateway at the ER membrane. Annu. Rev. Cell Dev. Biol. 15, 799-842 (1999).
2. Rapoport, T., Goder, V., Heinrich, S. & Matlack, K. Membrane-protein integration and the role of the translocation channel. Trends Cell Biol. 14, 568-575 (2004).
3. Menetret, J.-F. et al. Architecture of the ribosome-channel complex derived from native membranes. J. Mol. Biol. 348, 445-457 (2005).
4. Görlich, D. & Rapoport, T. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75, 615-630 (1993).
5. Crowley, K., Liao, S., Worrell, V., Reinhart, G. & Johnson, A. Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore. Cell 78, 461-471 (1994).
6. Van den Berg, B. et al. X-ray structure of a protein-conducting channel. Nature 427, 36-44 (2004).
7. High, S. et al. Site-specific photocrosslinking reveals that Sec61P and TRAM contact different regions of a membrane inserted signal sequence. J. Biol. Chem. 268, 26745-26751 (1993).
8. Thrift, R.N., Andrews, D.W., Walter, P. & Johnson, A.E. A nascent membrane protein is located adjacent to ER membrane proteins throughout its integration and translocation. J. Cell Biol. 112, 809-821 (1991).
9. Mothes, W., Prehn, S. & Rapoport, T. Systematic probing of the environment of a translocating secretory protein during translocation through the ER membrane. EMBO J. 13, 3973-3982 (1994).
10. McCormick, P., Miao, Y., Shao, Y., Lin, J. & Johnson, A. Cotranslational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Mol. Cell 12, 329-341 (2003).
11. Liao, S., Lin, J., Do, H. & Johnson, A. Both lumenal and cytosolic gating of the aqueous translocon pore are regulated from inside the ribosome during membrane protein integration. Cell 90, 31-42 (1997).
12. Woolhead, C., McCormick, P. & Johnson, A. Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116, 725-736 (2004).
13. High, S. et al. Sec61p is adjacent to nascent type I and type II signal-anchor proteins during their membrane insertion. J. Cell Biol. 121, 743-750 (1993).
14. Martoglio, B., Hofmann, M., Brunner, J. & Dobberstein, B. The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell 81, 207-214 (1995).
15. Do, H., Falcone, D., Lin, J., Andrews, D. & Johnson, A. The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell 85, 369-378 (1996).
16. Mothes, W. et al. Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell 89, 523-533 (1997).
17. Heinrich, S.U., Mothes, W., Brunner, J. & Rapoport, T. The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell 102, 233-244 (2000).
18. Meacock, S., Lecomte, F., Crawshaw, S. & High, S. Different transmembrane domains associate with distinct endoplasmic reticulum components during membrane integration of a polytopic protein. Mol. Biol. Cell 13, 4114-4129 (2002).
19. Heinrich, S. & Rapoport, T. Cooperation of transmembrane segments during integration of a double-spanning protein into the ER membrane. EMBO J. 22, 3654-3663 (2003).
20. Higy, M., Junne, T. & Spiess, M. Topogenesis of membrane proteins at the endoplasmic reticulum. Biochemistry 43, 12716-12722 (2004).
21. Alder, N. & Johnson, A. Cotranslational membrane protein biogenesis at the endoplasmic reticulum. J. Biol. Chem. 279, 22787-22790 (2004).
22. Sadlish, H. & Skach, W. Biogenesis of CFTR and other polytopic membrane proteins; new roles for the ribosome-translocon complex. J. Membr. Biol. 202, 115-126 (2004).
23. Skach, W. et al. Biogenesis and transmembrane topology of the CHIP28 water channel in the endoplasmic reticulum. J. Cell Biol. 125, 803-815 (1994).
24. Skach, W. & Lingappa, V. Amino terminus assembly of human P-glycoprotein at the endoplasmic reticulum is directed by cooperative actions of two internal sequences. J. Biol. Chem. 268, 23552-23561 (1993).
25. Lin, J. & Addison, R. A novel integration signal that is composed of two transmembrane segments is required to integrate the neorospora plasma membrane H+-ATPase into microsomes. J. Biol. Chem. 270, 6935-6941 (1995).
26. Borel, A. & Simon, S. Biogenesis of polytopic membrane proteins: membrane segments of P-glycoprotein sequentially translocate to span the ER membrane. Biochemistry 35, 10587-10594 (1996).
27. Hanein, D. et al. Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell 87, 721-732 (1996).
28. Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372 (2001).
29. Morgan, D., Menetret, J., Neuhof, A., Rapoport, T. & Akey, C. Structure of the mammalian ribosome-channel complex at 17A resolution. J. Mol. Biol. 324, 871-886 (2002).
30. Hegde, R. & Lingappa, V. Membrane protein biogenesis: regulated complexity at the endoplasmic reticulum. Cell 91, 575-582 (1997).
31. Bibi, E. The role of the ribosome-translocon complex in translation and assembly of polytopic membrane proteins. Trends Biochem. Sci. 23, 51-55 (1998).
32. Verkman, A. & Mitra, A. Structure and function of aquaporin water channels. Am. J. Physiol. Renal Physiol. 278, F13-F28 (2000).
33. Agre, P. et al. Aquaporin water channels - from atomic structure to clinical medicine. J. Physiol. (Lond.) 542, 3-16 (2002).
34. Fujiyoshi, Y. et al. Structure and function of water channels. Curr. Opin. Struct. Biol. 12, 509-515 (2002).
35. Sui, H., Han, B.-G., Lee, J., Walian, P. & Jap, B. Structural basis of water specific transport through the AQP1 water channel. Nature 414, 872-878 (2001).
36. Fu, D. et al. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290, 481-486 (2000).
37. Shi, L.-B., Skach, W., Ma, T. & Verkman, A. Distinct biogenesis mechanisms for water channels MIWC and CHIP28 at the endoplasmic reticulum. Biochemistry 34, 8250-8256 (1995).
38. Foster, W. et al. Identification of sequence determinants that direct different intracellular folding pathways for AQP1 and AQP4. J. Biol. Chem. 275, 34157-34165 (2000).
39. Nilsson, I. et al. Photocross-linking of nascent chains to the STT3 subunit of the oligosaccharyltransferase complex. J. Cell Biol. 161, 715-725 (2003).
40. Fons, R., Bogert, B. & Hegde, R. Substrate-specific function of the translocon-associated protein complex during translocation across the ER membrane. J. Cell Biol. 160, 529-539 (2003).
41. Wilson, C. et al. Ribophorin I associates with a subset of membrane proteins after their integration at the Sec61 translocon. J. Biol. Chem. 280, 4195-4206 (2005).
42. Snapp, E., Reinhart, G., Bogert, B., Lippencott-Schwartz, J. & Hegde, R. The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells. J. Cell Biol. 164, 997-1007 (2004).
43. Breyton, C., Haase, W., Rapoport, T., Kuehlbrandt, W. & Collinson, I. Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418, 662-665 (2002).
44. Manting, E., van der Does, C., Remigy, H., Engel, A. & Driessen, A. SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J. 19, 852-861 (2000).
45. Hamman, B., Chen, J.-C., Johnson, E. & Johnson, A. The aqueous pore through the translocon has a diameter of 40-60A during cotranslational protein translocation at the ER membrane. Cell 89, 535-544 (1997).
46. Moss, K., Helm, A., Lu, Y., Bragin, A. & Skach, W. Coupled translocation events generate topologic heterogeneity at the endoplasmic reticulum membrane. Mol. Biol. Cell 9, 2681-2697 (1998).
47. Carveth, K., Buck, T., Anthony, V. & Skach, W. Cooperativity and flexibility of cytsic fibrosis transmembrane conductance regulator transmembrane segments participate in membrane localization of a charged residue. J. Biol. Chem. 277, 39507-39514 (2002).
48. Goder, V., Bieri, C. & Spiess, M. Glycosylation can influence topogenesis of membrane proteins and reveals dynamic reorientation of nascent polypeptides within the translocon. J. Cell Biol. 147, 257-266 (1999).
49. Lu, Y. et al. Reorientation of Aquaporin-1 topology during maturation in the endoplasmic reticulum. Mol. Biol. Cell 11, 2973-2985 (2000).
50. Plath, K., Mothes, W., Wilkinson, B., Stirling, C. & Rapoport, T. Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807 (1998).