Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins

Cell

Volumn 116, Issue 5, 2004, Pages 725-736

  Woolhead, Cheryl A ^a,c   McCormick, Peter J ^b   Johnson, Arthur E ^a,b  

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

^b TEXAS A AND M UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CROSS LINKING; ENERGY TRANSFER; EUKARYOTE; FLUORESCENCE RESONANCE ENERGY TRANSFER; MEMBRANE POTENTIAL; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN FOLDING; RIBOSOME;

EUKARYOTA;

EID: 1542358892     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(04)00169-2     Document Type: Article

References (37)

1. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science. 289:2000;905-920.
2. Berisio R., Schlünzen F., Harms J., Bashan A., Auerbach T., Baram D., Yonath A. Structural insight into the role of the ribosomal tunnel in cellular regulation. Nat. Struct. Biol. 10:2003;366-370.
3. Crowley K.S., Reinhart G.D., Johnson A.E. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell. 73:1993;1101-1115.
4. Crowley K.S., Liao S., Worrell V.E., Reinhart G.D., Johnson A.E. Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore. Cell. 78:1994;461-471.
5. Dale R.E., Eisinger J., Blumberg W.E. The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer. Biophys. J. 26:1979;161-194.
6. Do H., Falcone D., Lin J., Andrews D.W., Johnson A.E. The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell. 85:1996;369-378.
7. Flanagan J.J., Chen J.-C., Miao Y., Shao Y., Lin J., Bock P.E., Johnson A.E. Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J. Biol. Chem. 278:2003;18628-18637.
8. Gabashvili I.S., Gregory S.T., Valle M., Grassucci R., Worbs M., Wahl M.C., Dahlberg A.E., Frank J. The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol. Cell. 8:2001;181-188.
9. Gong F., Yanofsky C. Instruction of translating ribosome by nascent peptide. Science. 297:2002;1864-1867.
10. Haigh N.G., Johnson A.E. A new role for BiP. Gating the aqueous ER translocon pore during membrane protein integration J. Cell Biol. 156:2002;261-270.
11. Hamman B.D., Chen J.-C., Johnson E.E., Johnson A.E. The aqueous pore through the translocon has a diameter of 40-60 Å during co-translational protein translocation at the ER membrane. Cell. 89:1997;535-544.
12. Hamman B.D., Hendershot L.M., Johnson A.E. BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell. 92:1998;747-758.
13. Hansen J.L., Ippolito J.A., Ban N., Nissen A., Moore P.B., Steitz T.A. The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol. Cell. 10:2002;117-128.
14. Hillel Z., Wu C.-W. Statistical interpretation of fluorescence energy transfer measurements in macromolecular systems. Biochemistry. 15:1976;2105-2113.
15. Johnson A.E., van Waes M.A. The translocon. a dynamic gateway at the ER membrane Annu. Rev. Cell Dev. Biol. 15:1999;799-842.
16. ε-acetyllysine transfer ribonucleic acid. A biologically active analogue of aminoacyl transfer ribonucleic acids Biochemistry. 15:1976;569-575.
17. Johnson A.E., Adkins H.J., Matthews E.A., Cantor C.R. Distance moved by transfer RNA during translocation from the A site to the P site on the ribosome. J. Mol. Biol. 156:1982;113-140.
18. Kramer G., Ramachandiran V., Hardesty B. Cotranslational folding - omnia mea mecum porto? Int. J. Biochem. Cell Biol. 33:2001;541-553.
19. Krieg U.C., Walter P., Johnson A.E. Photocrosslinking of the signal sequence of nascent preprolactin to the 54-kilodalton polypeptide of the signal recognition particle. Proc. Natl. Acad. Sci. USA. 83:1986;8604-8608.
20. Krieg U.C., Johnson A.E., Walter P. Protein translocation across the endoplasmic reticulum membrane. identification by photocross-linking of a 39 kD integral membrane glycoprotein as part of a putative translocation tunnel J. Cell Biol. 109:1989;2033-2043.
21. Liao S., Lin J., Do H., Johnson A.E. Both lumenal and cytosolic gating of the aqueous ER translocon pore is regulated from inside the ribosome during membrane protein integration. Cell. 90:1997;31-41.
22. McCormick P.J., Miao Y., Shao Y., Lin J., Johnson A.E. Cotranslational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Mol. Cell. 12:2003;329-341.
23. Mingarro I., Nilsson I., Whitley P., von Heijne G. Different conformations of nascent polypeptides during translocation across the ER membrane. BMC Cell Biol. 1:2000;3.
24. Mutucumarana V.P., Duffy E.J., Lollar P., Johnson A.E. The active site of factor IXa is located far above the membrane surface and its conformation is altered upon association with factor VIIIa. A fluorescence study. J. Biol. Chem. 267:1992;17012-17021.
25. Nakatogawa H., Ito K. The ribosomal exit tunnel functions as a discriminating gate. Cell. 108:2002;629-636.
26. Nissen P., Hansen J., Ban N., Moore P.B., Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science. 289:2000;920-930.
27. Schlünzen F., Zarivach R., Harms J., Bashan A., Tocilj A., Albrecht R., Yonath A., Franceschi F. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature. 413:2001;814-821.
28. Schnell D.J., Hebert D.N. Protein translocons. multifunctional mediators of protein translocation across membranes Cell. 112:2003;491-505.
29. Stryer L. Fluoresence energy transfer as a spectroscopic ruler. Annu. Rev. Biochem. 47:1978;819-846.
30. Tenson T., Ehrenberg M. Regulatory nascent peptides in the ribosomal tunnel. Cell. 108:2002;591-594.
31. van den Berg B., Clemons W.M. Jr., Collinson I., Modis Y., Hartmann E., Harrison S.C., Rapoport T.A. X-ray structure of a protein-conducting channel. Nature. 427:2004;36-44.
32. Watson B.S., Hazlett T.L., Eccleston J.F., Davis C., Jameson D.M., Johnson A.E. Macromolecular arrangement in the aminoacyl-tRNA•elongation factor Tu•GTP ternary complex. A fluorescence energy transfer study. Biochemistry. 34:1995;7904-7912.
33. Weber G., Teale F.W.J. Determination of the absolute quantum yield of fluorescent solutions. Trans. Faraday Soc. 53:1957;646-655.
34. Whitley P., Nilsson I., von Heijne G. A nascent secretory protein may traverse the ribosome/endoplasmic reticulum translocase complex as an extended chain. J. Biol. Chem. 271:1996;6241-6244.
35. Wirth A., Jung M., Bies C., Frien M., Tyedmers J., Zimmermann R., Wagner R. The Sec61p complex is a dynamic precursor activated channel. Mol. Cell. 12:2003;261-268.
36. Wu P., Brand L. Orientation factor in steady-state and time-resolved resonance energy transfer measurements. Biochemistry. 31:1992;7939-7947.
37. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H.D., Noller H.F. Crystal structure of the ribosome at 5.5 Å resolution. Science. 292:2001;883-896.