Home LiteratureArticle Details
PMID: 7744967 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Stage- and ribosome-specific alterations in nascent chain-Sec61p interactions accompany translocation across the ER membrane.

The Journal of cell biology ·Vol. 129 ·No. 4 ·1995-05-00 ·Pages 957-70

Nicchitta CV, Murphy EC, Haynes R, Shelness GS

Abstract

Near-neighbor interactions between translocating nascent chains and Sec61p were investigated by chemical cross-linking. At stages of translocation before signal sequence cleavage, nascent chains could be cross-linked to Sec61p at high (60-80%) efficiencies. Cross-linking occurred through the signal sequence and the mature portion of wild-type and signal cleavage mutant nascent chains. At later stages of translocation, as represented through truncated translocation intermediates, cross-linking to Sec61p was markedly reduced. Dissociation of the ribosome into its large and small subunits after assembly of the precursor into the translocon, but before cross-linking, resulted in a dramatic reduction in subsequent cross-linking yield, indicating that at early stages of translocation, nascent chain-Sec61p interactions are in part mediated through interactions of the ribosome with components of the ER membrane, such as Sec61p. Dissociation of the ribosome was, however, without effect on subsequent translocation. These results are discussed with respect to a model in which Sec61p performs a function essential for the initiation of protein translocation.

MeSH Terms
Base Sequence Biological Transport Cell Compartmentation Cross-Linking Reagents Endoplasmic Reticulum/metabolism Membrane Proteins/metabolism Membranes/metabolism Models, Genetic Molecular Sequence Data Peptides/metabolism Protein Binding Protein Biosynthesis Ribosomes/metabolism SEC Translocation Channels
Chemicals
Cross-Linking Reagents Membrane Proteins Peptides SEC Translocation Channels
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Nicchitta C V
Department of Cell Biology, Duke University Medical Center, Durham, North Carolina 27705, USA.
Murphy E C
Haynes R
Shelness G S
References (64)
64 references, click to expand
  1. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum.
    J Cell Biol. 1982 Apr;93(1):97-102 PMID: 7068762
  2. SecA protein is exposed to the periplasmic surface of the E. coli inner membrane in its active state.
    Cell. 1994 Sep 9;78(5):845-53 PMID: 8087851
  3. Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA.
    Methods Enzymol. 1983;96:50-74 PMID: 6656641
  4. Preparation of microsomal membranes for cotranslational protein translocation.
    Methods Enzymol. 1983;96:84-93 PMID: 6656655
  5. Uncoupling translocation from translation: implications for transport of proteins across membranes.
    Science. 1986 Apr 18;232(4748):348-52 PMID: 3961485
  6. A new method for predicting signal sequence cleavage sites.
    Nucleic Acids Res. 1986 Jun 11;14(11):4683-90 PMID: 3714490
  7. Formation of a functional ribosome-membrane junction during translocation requires the participation of a GTP-binding protein.
    J Cell Biol. 1986 Dec;103(6 Pt 1):2253-61 PMID: 3097028
  8. A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum.
    J Cell Biol. 1987 Aug;105(2):633-45 PMID: 3305520
  9. A signal sequence receptor in the endoplasmic reticulum membrane.
    Nature. 1987 Aug 27-Sep 2;328(6133):830-3 PMID: 3041222
  10. Evidence for the loop model of signal-sequence insertion into the endoplasmic reticulum.
    Proc Natl Acad Sci U S A. 1988 Oct;85(20):7592-6 PMID: 2845415
  11. Differences in the association of ribosomes with heavy rough and light rough endoplasmic reticulum membranes of MPC-11 cells.
    Biochim Biophys Acta. 1988 Nov 17;967(2):218-23 PMID: 2903770
  12. Access of proteinase K to partially translocated nascent polypeptides in intact and detergent-solubilized membranes.
    J Cell Biol. 1989 Feb;108(2):299-307 PMID: 2537313
  13. Nascent secretory chain binding and translocation are distinct processes: differentiation by chemical alkylation.
    J Cell Biol. 1989 Mar;108(3):789-95 PMID: 2537834
  14. 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. 1989 Nov;109(5):2033-43 PMID: 2808520
  15. Photocrosslinking demonstrates proximity of a 34 kDa membrane protein to different portions of preprolactin during translocation through the endoplasmic reticulum.
    FEBS Lett. 1989 Nov 6;257(2):263-8 PMID: 2583273
  16. Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum in yeast.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2641-52 PMID: 2687285
  17. SEC62 encodes a putative membrane protein required for protein translocation into the yeast endoplasmic reticulum.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2653-64 PMID: 2687286
  18. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins.
    Cell. 1990 Jan 26;60(2):271-80 PMID: 2153463
  19. The "megaprimer" method of site-directed mutagenesis.
    Biotechniques. 1990 Apr;8(4):404-7 PMID: 2340178
  20. Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast.
    J Cell Biol. 1990 Jun;110(6):1885-95 PMID: 2190988
  21. Cloning, in vitro transcription, and biological activity of Escherichia coli 23S ribosomal RNA.
    Nucleic Acids Res. 1990 Jun 25;18(12):3515-20 PMID: 2194163
  22. Ribonucleoparticle-independent import of proteins into mammalian microsomes involves a membrane protein which is sensitive to chemical alkylation.
    Biochimie. 1990 Feb-Mar;72(2-3):95-101 PMID: 2116185
  23. Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex.
    Nature. 1991 Feb 28;349(6312):806-8 PMID: 2000150
  24. A protein-conducting channel in the endoplasmic reticulum.
    Cell. 1991 May 3;65(3):371-80 PMID: 1902142
  25. ER translocation intermediates are adjacent to a nonglycosylated 34-kD integral membrane protein.
    J Cell Biol. 1991 Jul;114(1):21-33 PMID: 1646822
  26. Transcription of full-length and truncated mRNA transcripts to study protein translocation across the endoplasmic reticulum.
    Methods Cell Biol. 1991;34:223-39 PMID: 1943802
  27. Protein translocation mutants defective in the insertion of integral membrane proteins into the endoplasmic reticulum.
    Mol Biol Cell. 1992 Feb;3(2):129-42 PMID: 1550957
  28. The signal sequence receptor, unlike the signal recognition particle receptor, is not essential for protein translocation.
    J Cell Biol. 1992 Apr;117(1):15-25 PMID: 1313437
  29. Yeast Sec proteins interact with polypeptides traversing the endoplasmic reticulum membrane.
    Cell. 1992 Apr 17;69(2):343-52 PMID: 1568249
  30. Sec61p and BiP directly facilitate polypeptide translocation into the ER.
    Cell. 1992 Apr 17;69(2):353-65 PMID: 1568250
  31. A protein of the endoplasmic reticulum involved early in polypeptide translocation.
    Nature. 1992 May 7;357(6373):47-52 PMID: 1315422
  32. Signal peptides open protein-conducting channels in E. coli.
    Cell. 1992 May 15;69(4):677-84 PMID: 1375130
  33. Polypeptide translocation across the endoplasmic reticulum membrane.
    J Biol Chem. 1992 Jul 15;267(20):13791-4 PMID: 1321124
  34. Protein targeting to and translocation across the membrane of the endoplasmic reticulum.
    Curr Opin Cell Biol. 1992 Aug;4(4):573-80 PMID: 1419037
  35. A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation.
    Cell. 1992 Oct 30;71(3):489-503 PMID: 1423609
  36. Transport of proteins across the endoplasmic reticulum membrane.
    Science. 1992 Nov 6;258(5084):931-6 PMID: 1332192
  37. Reconstitution of protein translocation from solubilized yeast membranes reveals topologically distinct roles for BiP and cytosolic Hsc70.
    J Cell Biol. 1993 Jan;120(1):95-102 PMID: 8416998
  38. The SecA and SecY subunits of translocase are the nearest neighbors of a translocating preprotein, shielding it from phospholipids.
    EMBO J. 1993 Jan;12(1):255-63 PMID: 8428583
  39. Human coagulation factor X deficiency caused by a mutant signal peptide that blocks cleavage by signal peptidase but not targeting and translocation to the endoplasmic reticulum.
    J Biol Chem. 1993 Mar 15;268(8):5735-40 PMID: 8449937
  40. Sec61p is adjacent to nascent type I and type II signal-anchor proteins during their membrane insertion.
    J Cell Biol. 1993 May;121(4):743-50 PMID: 8491769
  41. Lumenal proteins of the mammalian endoplasmic reticulum are required to complete protein translocation.
    Cell. 1993 Jun 4;73(5):989-98 PMID: 8500184
  42. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation.
    Cell. 1993 Jun 18;73(6):1101-15 PMID: 8513496
  43. A tetrameric complex of membrane proteins in the endoplasmic reticulum.
    Eur J Biochem. 1993 Jun 1;214(2):375-81 PMID: 7916687
  44. SecA protein is required for translocation of a model precursor protein into inverted vesicles of Escherichia coli plasma membrane.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9011-5 PMID: 8415645
  45. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane.
    Cell. 1993 Nov 19;75(4):615-30 PMID: 8242738
  46. The signal sequence receptor has a second subunit and is part of a translocation complex in the endoplasmic reticulum as probed by bifunctional reagents.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2283-94 PMID: 2177473
  47. A nascent membrane protein is located adjacent to ER membrane proteins throughout its integration and translation.
    J Cell Biol. 1991 Mar;112(5):809-21 PMID: 1999459
  48. Unfolding of Escherichia coli ribosomes by removal of magnesium.
    J Mol Biol. 1966 Jul;18(2):356-71 PMID: 4961271
  49. On the attachment of ribosomes to microsomal membranes.
    J Mol Biol. 1966 Aug;19(2):503-24 PMID: 4961331
  50. Partial resistance of nascent polypeptide chains to proteolytic digestion due to ribosomal shielding.
    J Mol Biol. 1967 Jun 14;26(2):329-46 PMID: 4962271
  51. Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components.
    J Cell Biol. 1975 Dec;67(3):852-62 PMID: 811672
  52. The application of chemical crosslinking for studies on cell membranes and the identification of surface reporters.
    Biochim Biophys Acta. 1979 Apr 23;559(1):39-69 PMID: 156043
  53. 3-Trifluoromethyl-3-phenyldiazirine. A new carbene generating group for photolabeling reagents.
    J Biol Chem. 1980 Apr 25;255(8):3313-8 PMID: 7364745
  54. Intracellular protein topogenesis.
    Proc Natl Acad Sci U S A. 1980 Mar;77(3):1496-500 PMID: 6929499
  55. Site-specific photocross-linking reveals that Sec61p and TRAM contact different regions of a membrane-inserted signal sequence.
    J Biol Chem. 1993 Dec 15;268(35):26745-51 PMID: 8253810
  56. Suppression of a sec63 mutation identifies a novel component of the yeast endoplasmic reticulum translocation apparatus.
    Mol Biol Cell. 1993 Sep;4(9):919-30 PMID: 8257794
  57. Structural and functional characterization of Sec66p, a new subunit of the polypeptide translocation apparatus in the yeast endoplasmic reticulum.
    Mol Biol Cell. 1993 Sep;4(9):931-9 PMID: 8257795
  58. The membrane proteins TRAMp and sec61 alpha p may be involved in post-translational transport of presecretory proteins into mammalian microsomes.
    FEBS Lett. 1994 Mar 21;341(2-3):281-7 PMID: 8137954
  59. Binding of ribosomes to the rough endoplasmic reticulum mediated by the Sec61p-complex.
    J Cell Biol. 1994 Aug;126(4):925-34 PMID: 8051212
  60. Sec72p contributes to the selective recognition of signal peptides by the secretory polypeptide translocation complex.
    J Cell Biol. 1994 Aug;126(4):935-43 PMID: 8051213
  61. Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore.
    Cell. 1994 Aug 12;78(3):461-71 PMID: 8062388
  62. Systematic probing of the environment of a translocating secretory protein during translocation through the ER membrane.
    EMBO J. 1994 Sep 1;13(17):3973-82 PMID: 8076593
  63. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion.
    Cell. 1994 Sep 9;78(5):835-43 PMID: 8087850
  64. Structural properties of homogeneous protein disulphide-isomerase from bovine liver purified by a rapid high-yielding procedure.
    Biochem J. 1983 Jul 1;213(1):225-34 PMID: 6615424
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1995-05-00
Pages
957-70
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120490
Subset
IM
Grants
NHLBI NIH HHS · P01 HL 49373 · United States
NIDDK NIH HHS · R01 DK 47897 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com