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PMID: 11739803 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Lipid composition of outer leaflet of chloroplast outer envelope determines topology of OEP7.

Molecular biology of the cell ·Vol. 12 ·No. 12 ·2001-12-00 ·Pages 4090-102

Schleiff E, Tien R, Salomon M, Soll J

Abstract

OEP7, a 6.7-kDa outer envelope protein of spinach chloroplasts inserts into the outer envelope of the organelle independent of a classical cleavable targeting signal. The insertion of OEP7 was studied to describe the determinants for association with, integration into, and orientation of the protein in the outer envelope of chloroplasts. The insertion of OEP7 into the membrane is independent of outer membrane channel proteins and can be reconstituted with the use of protein-free liposomes. In situ, the binding of OEP7 to the membrane surface is not driven by electrostatic interaction because reduction of phosphatidylglycerol or phosphatidylinositol did not reduce the association with the liposomes. The positively charged amino acids flanking the transmembrane domain at the C terminus are essential to retain the native N(in)-C(out) orientation during insertion into chloroplasts. OEP7 inserts with reversed orientation into liposomes containing the average lipid composition of the outer envelopes. The native like N(in)-C(out) orientation is achieved by reduction of the phoshpatidylglycerol concentration mimicking the composition of the outer leaflet of the outer envelope of chloroplasts. We conclude that the unique lipid composition of the outer leaflet due to lipid asymmetry of the outer envelope is essential for the correct topology of OEP7.

MeSH Terms
Chloroplasts/chemistry Hydrophobic and Hydrophilic Interactions Liposomes/chemistry,metabolism Membrane Lipids/analysis,metabolism Membrane Proteins/chemistry,genetics,metabolism Models, Biological Phosphatidylglycerols/metabolism Phosphatidylinositols/metabolism Plant Proteins/chemistry,genetics,metabolism Protein Conformation Spinacia oleracea/genetics Static Electricity Thermodynamics
Chemicals
Liposomes Membrane Lipids Membrane Proteins Phosphatidylglycerols Phosphatidylinositols Plant Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Schleiff E
Botanisches Institut, Universität Kiel, 24118 Kiel, Germany.
Tien R
Salomon M
Soll J
References (55)
55 references, click to expand
  1. Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease.
    EMBO J. 1998 Sep 15;17(18):5255-64 PMID: 9736605
  2. Anionic phospholipids modulate peptide insertion into membranes.
    Biochemistry. 1997 May 6;36(18):5476-82 PMID: 9154930
  3. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS.
    Plant Physiol. 1949 Jan;24(1):1-15 PMID: 16654194
  4. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels.
    Eur J Biochem. 1974 Jul 1;46(1):83-8 PMID: 4850204
  5. Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results.
    Biophys J. 1996 Aug;71(2):561-75 PMID: 8842196
  6. Small-volume extrusion apparatus for preparation of large, unilamellar vesicles.
    Biochim Biophys Acta. 1991 Jan 30;1061(2):297-303 PMID: 1998698
  7. Hydrophobic interactions of peptides with membrane interfaces.
    Biochim Biophys Acta. 1998 Nov 10;1376(3):339-52 PMID: 9804985
  8. Membrane association of FtsY, the E. coli SRP receptor.
    FEBS Lett. 1997 Oct 27;416(3):225-9 PMID: 9373157
  9. Insertion of atToc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system.
    J Biol Chem. 1999 Jun 25;274(26):18735-40 PMID: 10373488
  10. Characterization and isolation of the chloroplast protein import machinery.
    Methods Cell Biol. 1995;50:255-67 PMID: 8531798
  11. Electrostatics and the membrane association of Src: theory and experiment.
    Biochemistry. 1998 Feb 24;37(8):2145-59 PMID: 9485361
  12. Thermodynamics of the alpha-helix-coil transition of amphipathic peptides in a membrane environment: implications for the peptide-membrane binding equilibrium.
    J Mol Biol. 1999 Dec 3;294(3):785-94 PMID: 10610796
  13. Sequence analysis and protein import studies of an outer chloroplast envelope polypeptide.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5778-82 PMID: 2377616
  14. Non-bilayer lipids are required for efficient protein transport across the plasma membrane of Escherichia coli.
    EMBO J. 1995 Nov 15;14(22):5506-13 PMID: 8521807
  15. The transit sequence of a chloroplast precursor protein reorients the lipids in monogalactosyl diglyceride containing bilayers.
    FEBS Lett. 1994 Aug 15;350(1):104-8 PMID: 8062905
  16. Biochemistry and function of the plastid envelope.
    Annu Rev Cell Biol. 1990;6:173-216 PMID: 2275813
  17. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.
    Anal Biochem. 1987 Nov 1;166(2):368-79 PMID: 2449095
  18. Site of biosynthesis of galactolipids in spinach chloroplasts.
    Science. 1974 Mar 1;183(4127):852-3 PMID: 17780772
  19. Calculations of the electrostatic potential adjacent to model phospholipid bilayers.
    Biophys J. 1995 Mar;68(3):729-38 PMID: 7756540
  20. Free-energy determinants of alpha-helix insertion into lipid bilayers.
    Biophys J. 1996 Apr;70(4):1803-12 PMID: 8785340
  21. Localization of phosphatidylcholine in outer envelope membrane of spinach chloroplasts.
    J Cell Biol. 1985 May;100(5):1690-7 PMID: 3988805
  22. The Galactolipid, Phospholipid, and Fatty Acid Composition of the Chloroplast Envelope Membranes of Vicia faba. L.
    Plant Physiol. 1974 Mar;53(3):496-502 PMID: 16658731
  23. The role of lipids in plastid protein transport.
    Plant Mol Biol. 1998 Sep;38(1-2):223-46 PMID: 9738969
  24. Phosphatidylethanolamine mediates insertion of the catalytic domain of leader peptidase in membranes.
    FEBS Lett. 1998 Jul 10;431(1):75-9 PMID: 9684869
  25. Positively and negatively charged residues have different effects on the position in the membrane of a model transmembrane helix.
    J Mol Biol. 1998 Dec 11;284(4):1177-83 PMID: 9837735
  26. Outer envelope membranes from chloroplasts are isolated as right-side-out vesicles.
    Planta. 1992 Apr;187(1):89-94 PMID: 24177971
  27. A constituent of the chloroplast import complex represents a new type of GTP-binding protein.
    Plant J. 1995 Mar;7(3):401-11 PMID: 7757113
  28. Functional domains of the ferredoxin transit sequence involved in chloroplast import.
    J Biol Chem. 1995 Feb 24;270(8):3882-93 PMID: 7876133
  29. A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A.
    Nature. 1991 Dec 5;354(6352):408-10 PMID: 1956406
  30. Insertion of the 34-kDa chloroplast protein import component, IAP34, into the chloroplast outer membrane is dependent on its intrinsic GTP-binding capacity.
    J Biol Chem. 1997 Mar 7;272(10):6614-20 PMID: 9045691
  31. Positive charges determine the topology and functionality of the transmembrane domain in the chloroplastic outer envelope protein Toc34.
    J Cell Biol. 1998 May 18;141(4):895-904 PMID: 9585409
  32. Localization of polypeptides to the cytosolic side of the outer envelope membrane of spinach chloroplasts.
    J Biol Chem. 1983 Aug 25;258(16):10000-6 PMID: 6350279
  33. Continuum solvent model calculations of alamethicin-membrane interactions: thermodynamic aspects.
    Biophys J. 2000 Feb;78(2):571-83 PMID: 10653772
  34. Slow Passive Diffusion of Orthophosphate between Intact Isolated Chloroplasts and Suspending Medium.
    Plant Physiol. 1981 Mar;67(3):470-3 PMID: 16661696
  35. Travelling of proteins through membranes: translocation into chloroplasts.
    Planta. 2000 Sep;211(4):449-56 PMID: 11030543
  36. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins.
    Annu Rev Biophys Biophys Chem. 1986;15:321-53 PMID: 3521657
  37. Protein translocation into and across the chloroplastic envelope membranes.
    Plant Mol Biol. 1998 Sep;38(1-2):191-207 PMID: 9738967
  38. A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway.
    EMBO J. 1995 Jun 1;14(11):2436-46 PMID: 7781598
  39. Identification of two GTP-binding proteins in the chloroplast protein import machinery.
    Science. 1994 Nov 11;266(5187):1035-9 PMID: 7973656
  40. Protein import and routing systems of chloroplasts.
    Plant Cell. 1999 Apr;11(4):557-70 PMID: 10213778
  41. A simple, sensitive method for lipid phosphorus.
    Lipids. 1974 Jul;9(7):491-2 PMID: 4407655
  42. Statistical thermodynamic analysis of peptide and protein insertion into lipid membranes.
    Biophys J. 1996 Jul;71(1):130-7 PMID: 8804596
  43. Protein targeting and integration signal for the chloroplastic outer envelope membrane.
    Plant Cell. 1996 Nov;8(11):2117-26 PMID: 8953775
  44. Anionic phospholipids are involved in membrane association of FtsY and stimulate its GTPase activity.
    EMBO J. 2000 Feb 15;19(4):531-41 PMID: 10675322
  45. Reconstitution of a chloroplast protein import channel.
    EMBO J. 1997 Dec 15;16(24):7351-60 PMID: 9405364
  46. Insertion of OEP14 into the outer envelope membrane is mediated by proteinaceous components of chloroplasts.
    Plant Cell. 2000 Oct;12(10):1951-60 PMID: 11041889
  47. Phospholipid-assisted refolding of an integral membrane protein. Minimum structural features for phosphatidylethanolamine to act as a molecular chaperone.
    J Biol Chem. 1999 Apr 30;274(18):12339-45 PMID: 10212204
  48. The transit sequence mediates the specific interaction of the precursor of ferredoxin with chloroplast envelope membrane lipids.
    J Biol Chem. 1993 Feb 25;268(6):4037-42 PMID: 8440696
  49. Hydrophobic forces drive spontaneous membrane insertion of the bacteriophage Pf3 coat protein without topological control.
    EMBO J. 1999 Nov 15;18(22):6299-306 PMID: 10562542
  50. Binding of peptides with basic residues to membranes containing acidic phospholipids.
    Biophys J. 1991 Jul;60(1):135-48 PMID: 1883932
  51. Polypeptide composition of envelopes of spinach chloroplasts: two major proteins occupy 90% of outer envelope membranes.
    Plant Cell Physiol. 1998 May;39(5):526-32 PMID: 9664716
  52. Direct membrane insertion of voltage-dependent anion-selective channel protein catalyzed by mitochondrial Tom20.
    J Cell Biol. 1999 May 31;145(5):973-8 PMID: 10352015
  53. A novel chloroplastic outer membrane-targeting signal that functions at both termini of passenger polypeptides.
    J Biol Chem. 1997 Apr 18;272(16):10968-74 PMID: 9099756
  54. Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts.
    Plant Cell. 1991 Jul;3(7):709-17 PMID: 1841725
  55. Lipid-peptide interactions between fragments of the transit peptide of ribulose-1,5-bisphosphate carboxylase/oxygenase and chloroplast membrane lipids.
    FEBS Lett. 1991 Oct 21;291(2):350-4 PMID: 1936285
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2001-12-00
Pages
4090-102
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC60778
Subset
IM
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