The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum

Journal of Cell Biology

Volumn 168, Issue 3, 2005, Pages 389-399

  Alder, Nathan N ^a   Shen, Ying ^b,c   Brodsky, Jeffrey L ^d   Hendershot, Linda M ^b,c   Johnson, Arthur E ^a,e  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; FLUORESCENT DYE; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN 70; MEMBRANE PROTEIN; TRANSLOCON;

ARTICLE; BINDING SITE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; MICROSOME; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; BINDING, COMPETITIVE; CRICETINAE; ENDOPLASMIC RETICULUM; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; FUNGAL PROTEINS; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; IODINE; MEMBRANE PROTEINS; MICROSOMES; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; MUTATION; PEPTIDES; PROLACTIN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PRECURSORS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SPECTROMETRY, FLUORESCENCE;

PHOCIDAE;

EID: 13444271726     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200409174     Document Type: Article

References (53)

1. Alder, N.N., and A.E. Johnson. 2004. Cotranslational membrane protein biogenesis at the endoplasmic reticulum. J. Biol. Chem. 279:22787-22790.
2. Beckmann, R., D. Bubeck, R. Grassucci, P. Penczek, A. Verschoor, G. Blobel, and J. Frank. 1997. Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex. Science. 278:2123-2126.
3. Bertolotti, A., Y. Zhang, L.M. Hendershot, H.P. Harding, and D. Ron. 2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2:326-332.
4. Brodsky, J.L., J. Goeckeler, and R. Schekman. 1995. BiP and Sec63p are required for both co- and post-translational protein translocation into the yeast endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 92:9643-9646.
5. Brodsky, J.L., M. Bäuerle, M. Horst, and A.J. McClellan. 1998. Mitochondrial Hsp70 cannot replace BiP in driving protein translocation into the yeast endoplasmic reticulum. FEBS Lett. 435:183-186.
6. Bukau, B., and A.L. Horwich. 1998. The Hsp70 and Hsp60 chaperone machines. Cell. 92:351-366.
7. Bulleid, N.J., and R.B. Freedman. 1988. Defective co-translational formation of disulphide bonds in protein disulphide-isomerase-deficient microsomes. Nature. 335:649-651.
8. Chavalier, M., H. Rhee, E.C. Elguindi, and S.Y. Blond. 2000. Interaction of murine BiP/GRP78 with the DnaJ homologue MTJ1. J. Biol. Chem. 275:19620-19627.
9. Chung, K.T., Y. Shen, and L.M. Hendershot. 2002. BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J. Biol. Chem. 277:47557-47563.
10. Corsi, A.K., and R. Schekman. 1997. The lumenal domain of Sec63p stimulates the ATPase activity of BiP and mediates BiP recruitment to the translocon in Saccharomyces cerevisiae. J. Cell Biol. 137:1483-1493.
11. Crowley, K.S., G.D. Reinhart, and A.E. Johnson. 1993. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell. 73:1101-1115.
12. Crowley, K.S., S. Liao, V.E. Worrell, G.D. Reinhart, and A.E. Johnson. 1994. Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore. Cell. 78:461-471.
13. Dudek, J., J. Volkmer, C. Bies, S. Guth, A. Müller, M. Lerner, P. Feick, K.-H. Schäfer, E. Morgenstern, F. Hennessy, et al. 2002. A novel type of co-chaperone mediates transmembrane recruitment of DnaK-like chaperones to ribosomes. EMBO J. 21:2958-2967.
14. Fiske, C.H., and Y. Subbarow. 1925. The colorimetric determination of phosphorus. J. Biol. Chem. 66:375-400.
15. Flynn, G.C., T.G. Chappell, and J.E. Rothman. 1989. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science. 245:385-390.
16. Gaut, J.R., and L.M. Hendershot. 1993. Mutations within the nucleotide binding site of immunoglobulin-binding protein inhibit ATPase activity and interfere with release of immunoglobulin heavy chain. J. Biol. Chem. 268:7248-7255.
17. Greene, M.K., K. Maskos, and S.L. Landry. 1998. Role of the J-domain in the cooperation of Hsp40 with Hsp70. Proc. Natl. Acad. Sci. USA. 95:6108-6113.
18. Haigh, N.G., and A.E. Johnson. 2002. A new role for BiP: closing the aqueous translocon pore during protein integration into the ER membrane. J. Cell Biol. 156:261-270.
19. Hamman, B.D., J.-C. Chen, E.E. Johnson, and A.E. Johnson. 1997. The aqueous pore through the translocon has a diameter of 40-60 Å during cotranslational protein translocation at the ER membrane. Cell. 89:535-544.
20. Hamman, B.D., L.M. Hendershot, and A.E. Johnson. 1998. BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell. 92:747-758.
21. Hanein, D., K.E. Matlack, B. Jungnickel, K. Plath, K.U. Kalies, K.R. Miller, T.A. Rapoport, and C.W. Akey. 1996. Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell. 87:721-732.
22. Hendershot, L., J. Wei, J. Gaut, J. Melnick, S. Aviel, and Y. Argon. 1996. Inhibition of immunoglobulin folding and secretion by dominant negative BiP ATPase mutants. Proc. Natl. Acad. Sci. USA. 93:5269-5274.
23. Höhfeld, J., Y. Minami, and F.U. Hartl. 1995. Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell. 83:589-598.
24. Johnson, A.E., and M.A. van Waes. 1999. The translocon: a dynamic gateway at the ER membrane. Annu. Rev. Cell Dev. Biol. 15:799-842.
25. Kabani, M., S.S. Kelley, M.W. Morrow, D.L. Montgomery, R. Sivendran, M.D. Rose, L.M. Gierasch, and J.L. Brodsky. 2003. Dependence of endoplasmic reticulum-associated degradation on the peptide binding domain and concentration of BiP. Mol. Biol. Cell. 14:3437-3448.
26. Kimata, Y., Y.I. Kimata, Y. Shimizu, H. Abe, I.C. Farcasanu, M. Takeuchi, M.D. Rose, and K. Kohno. 2003. Genetic evidence for a role of BiP/Kar2 that regulates Ire 1 in response to accumulation of unfolded proteins. Mol Biol. Cell. 14:2559-2569.
27. Ladokhin, A.S., M.E. Selsted, and S.H. White. 1997. Sizing membrane pores in lipid vesicles by leakage of co-encapsulated markers: pore formation by melittin. Biophys. J. 72:1762-1766.
28. Levy, R., M. Wiedmann, and G. Kreibich. 2001. In vitro binding of ribosomes to the β subunit of the Sec61p protein translocation complex. J. Biol. Chem. 276:2340-2346.
29. Liao, S., J. Lin, H. Do, and A.E. Johnson. 1997. Both lumenal and cytosolic gating of the aqueous ER translocon pore is regulated from inside the ribosome during membrane protein integration. Cell. 90:31-41.
30. Ma, K., K.M. Vattem, and R.C. Wek. 2002. Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 kinase in response to endoplasmic reticulum stress. J. Biol. Chem. 277:18728-18735.
31. Matlack, K.E., B. Misselwitz, K. Plath, and T.A. Rapoport. 1999. BiP acts as a molecular ratchet during posttranslational transport of prepro-α factor across the ER membrane. Cell. 97:553-564.
32. Mayer, M., J. Reinstein, and J. Buchner. 2003. Modulation of the ATPase cycle of BiP by peptides and proteins. J. Mol. Biol. 330:137-144.
33. McClellan, A.J., J.B. Endres, J.P. Vogel, D. Palazzi, M.D. Rose, and J.L. Brodsky. 1998. Specific molecular chaperone interactions and an ATP-dependent conformational change are required during posttranslational protein translocation into the yeast ER. Mol. Biol. Cell. 9:3533-3545.
34. Meyer, H.A., H. Grau, R. Kraft, S. Kostka, S. Prehn, K.U. Kalies, and E. Hartmann. 2000. Mammalian Sec61 is associated with Sec62 and Sec63. J. Biol. Chem. 275:14550-14557.
35. Miller, M., A.J. Jermy, G.J. Steel, H.J. Garside, S. Carter, and C.J. Stirling. 2003. An in vitro assay using overexpressed yeast SRP demonstrates that cotranslational translocation is dependent upon the J-domain of Sec63p. Biochemistry. 42:7171-7177.
36. Misselwitz, B., O. Staeck, and T.A. Rapoport. 1998. J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences. Mol. Cell. 2:593-603.
37. Misselwitz, B., O. Staeck, K.E. Matlack, and T.A. Rapoport. 1999. Interaction of BiP with the J-domain of the Sec61p component of the endoplasmic reticulum protein translocation complex. J. Biol. Chem. 274:20110-20115.
38. Nicchitta, C.V., and G. Blobel. 1993. Lumenal proteins of the mammalian endoplasmic reticulum are required to complete protein translocation. Cell. 73:989-998.
39. Raden, D., W. Song, and R. Gilmore. 2000. Role of the cytoplasmic segments of Sed61a in the ribosome-binding and translocation-promoting activities of the Sec61 complex. J. Cell Biol. 150:53-64.
40. Shen, J., X. Chen, L.M. Hendershot, and R. Prywes. 2002. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell. 3:99-111.
41. Shen, Y., L. Meunier, and L.M. Hendershot. 2002. Identification and characterization of a novel endoplasmic reticulum (ER) DnaJ homologue, which stimulates ATPase activity of BiP in vitro and is induced by ER stress. J. Biol. Chem. 277:15947-15956.
42. Simon, S.M., and G. Blobel. 1991. A protein-conducting channel in the endoplasmic reticulum. Cell. 65:371-380.
43. Suh, W.-C., W.F. Burkholder, C.Z. Lu, X. Zhao, M.E. Gottesman, and C.A. Gross. 1998. Interaction of the Hsp70 molecular chaperone, DnaK, with its cochaperone DnaJ. Proc. Natl. Acad. Sci. USA. 95:15223-15228.
44. Theyssen, H., H.P. Schuster, L. Packschies, B. Bukau, and J. Reinstein. 1996. The second step of ATP binding induces peptide release. J. Mol. Biol. 263:657-670.
45. Tyedmers, J., M. Lerner, C. Bies, J. Dudek, M.H. Skowronek, I.G. Haas, N. Heim, W. Nastainczyk, J. Volkmer, and R. Zimmermann. 2000. Homologs of the yeast Sec complex subunits Sec62p and Sec63p are abundant proteins in dog pancreas microsomes. Proc. Natl. Acad. Sci. USA. 97:7214-7219.
46. Vanhove, M., Y.-K. Usherwood, and L.M. Hendershot. 2001. Unassembled Ig heavy chains do not cycle from BiP in vivo, but require light chains to trigger their release. Immunity. 15:105-114.
47. Walter, P., and G. Blobel. 1983. Preparation of microsomal membranes for cotranslational protein translocation. Methods Enzymol. 96:84-93.
48. Wei, J., J.R. Gaut, and L.M. Hendershot. 1995. In vitro dissociation of BiP-peptide complexes requires a conformational change in BiP after ATP binding but does not require ATP hydrolysis. J. Biol. Chem. 270:26677-26682.
49. Wirth, A., M. Jung, C. Bies, M. Frien, J. Tyedmers, R. Zimmermann, and R. Wagner. 2003. The Sec61p complex is a dynamic precursor activated channel. Mol. Cell. 12:261-268.
50. Woolhead, C., P.J. McCormick, and A.E. Johnson. 2004. Nascent membrane and secretory proteins differ in their FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell. 116:725-736.
51. Young, B.P., R.A. Craven, P.J. Reid, M. Wilier, and C.J. Stirling. 2001. Sec63p and Kar2p are required for the translocation of SRP-dependent precursors into the yeast endoplasmic reticulum in vivo. EMBO J. 20:262-271.
52. Yu, M., R.H.A. Haslam, and D.B. Haslam. 2000. HEDJ, an Hsp40 co-chaperone localized to the endoplasmic reticulum of human cells. J. Biol. Chem. 275:24984-24992.
53. Zhu, X., X. Zhao, W.F. Burkholder, A. Gragerov, C.M. Ogata, M.E. Gottesman, and W.A. Hendrickson. 1996. Structural analysis of substrate binding by the molecular chaperone DnaK. Science. 272:1606-1614.