Abstract
We have used a cytosol-free assay in which efficient translocation and signal peptide cleavage is achieved when the affinity-purified precursor of OmpA (proOmpA) is diluted out of 8 M urea into a suspension of yeast rough microsomes. This aspect of protein targeting and transport occurs in two discernible steps: (a) in the absence of ATP and cytosolic factors, the precursor binds to the membranes but is not translocated; (b) addition of ATP results in the translocation of the bound precursor and its processing to the mature form. The binding to microsomes of radiolabeled proOmpA is saturable and inhibited by the addition of unlabeled proOmpA but not by mature OmpA or other proteins. The binding of radiolabeled prepro-alpha-factor is also effectively competed by other preproteins, but not by mature ones. Scatchard analysis showed the Kd of proOmpA to be 7.5 X 10(-9) M. Binding is most likely protein mediated as treatment of the microsomes with the protease papain was found to be inhibitory. These results represent the first functional characterization of secretory protein precursor binding to membranes. Alkylation of the microsomes with NEM, washing the membranes with urea or using membranes from the (translocation) mutant ptll at the nonpermissive temperature, did not affect binding, but did eliminate the subsequent ATP-dependent translocation. The ability to subdivide translocation into individual reactions provides a more precise means of determining the membrane components involved in this process.
MeSH Terms
Adenosine Triphosphate/metabolism
Bacterial Outer Membrane Proteins/metabolism
Biological Transport, Active/drug effects
Ethylmaleimide/pharmacology
Fungal Proteins/metabolism
In Vitro Techniques
Intracellular Membranes/metabolism
Kinetics
Mating Factor
Microsomes/metabolism
Papain/pharmacology
Peptides/metabolism
Protein Precursors/metabolism
Protein Processing, Post-Translational/drug effects
Receptors, Cell Surface/physiology
Saccharomyces cerevisiae
Chemicals
Bacterial Outer Membrane Proteins
Fungal Proteins
Peptides
Protein Precursors
Receptors, Cell Surface
Mating Factor
Adenosine Triphosphate
Papain
Ethylmaleimide
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sanz P
Department of Biological Chemistry, University of California, Los Angeles School of Medicine 90024.
Meyer D I
References (24)
24 references, click to expand
-
Signal recognition particle (SRP) stabilizes the translocation-competent conformation of pre-secretory proteins.
EMBO J. 1988 Nov;7(11):3553-7
PMID: 2850167
-
ProOmpA spontaneously folds in a membrane assembly competent state which trigger factor stabilizes.
EMBO J. 1988 Jun;7(6):1831-5
PMID: 3049077
-
In vivo and in vitro analysis of ptl1, a yeast ts mutant with a membrane-associated defect in protein translocation.
EMBO J. 1988 Dec 20;7(13):4347-53
PMID: 3072198
-
Preprotein conformation: the year's major theme in translocation studies.
Trends Biochem Sci. 1988 Dec;13(12):471-4
PMID: 2855285
-
Secretion in yeast: translocation and glycosylation of prepro-alpha-factor in vitro can occur via an ATP-dependent post-translational mechanism.
EMBO J. 1986 May;5(5):1031-6
PMID: 15957217
-
Secretion in yeast: reconstitution of the translocation and glycosylation of alpha-factor and invertase in a homologous cell-free system.
Cell. 1986 Feb 28;44(4):619-28
PMID: 3512097
-
In vitro protein translocation across the yeast endoplasmic reticulum: ATP-dependent posttranslational translocation of the prepro-alpha-factor.
Cell. 1986 May 9;45(3):397-406
PMID: 3009026
-
Both ATP and the electrochemical potential are required for optimal assembly of pro-OmpA into Escherichia coli inner membrane vesicles.
Proc Natl Acad Sci U S A. 1986 Jun;83(12):4219-22
PMID: 2872675
-
Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose-binding protein in E. coli.
Cell. 1986 Sep 12;46(6):921-8
PMID: 3530497
-
Transfer of secretory proteins through the membrane of the endoplasmic reticulum.
Int Rev Cytol. 1986;102:215-42
PMID: 3021646
-
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
-
Mechanism of protein translocation across the endoplasmic reticulum membrane.
Annu Rev Cell Biol. 1986;2:499-516
PMID: 3030381
-
Trigger factor: a soluble protein that folds pro-OmpA into a membrane-assembly-competent form.
Proc Natl Acad Sci U S A. 1987 Aug;84(15):5216-20
PMID: 3299381
-
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
-
A signal sequence receptor in the endoplasmic reticulum membrane.
Nature. 1987 Aug 27-Sep 2;328(6133):830-3
PMID: 3041222
-
Identification of a receptor for protein import into chloroplasts and its localization to envelope contact zones.
Nature. 1988 Jan 21;331(6153):232-7
PMID: 2827037
-
Secretion in yeast: structural features influencing the post-translational translocation of prepro-alpha-factor in vitro.
EMBO J. 1987 Nov;6(11):3455-63
PMID: 3322808
-
Protein unfolding and the energetics of protein translocation across biological membranes.
Cell. 1988 Feb 26;52(4):481-3
PMID: 3277719
-
A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides.
Nature. 1988 Apr 28;332(6167):800-5
PMID: 3282178
-
70K heat shock related proteins stimulate protein translocation into microsomes.
Nature. 1988 Apr 28;332(6167):805-10
PMID: 3282179
-
The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein.
Cell. 1988 Apr 22;53(2):273-83
PMID: 2834066
-
Import of honeybee prepromelittin into the endoplasmic reticulum: energy requirements for membrane insertion.
EMBO J. 1988 Mar;7(3):639-48
PMID: 3396536
-
Import of proteins into mitochondria: a multi-step process.
Eur J Biochem. 1988 Aug 1;175(2):205-12
PMID: 3042397
-
Nascent secretory chain binding and translocation are distinct processes: differentiation by chemical alkylation.
J Cell Biol. 1989 Mar;108(3):789-95
PMID: 2537834