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EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Biogenesis and Membrane Targeting of Lipoproteins

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  • Authors: Shin-Ichiro Narita1, and Hajime Tokuda2
  • Editors: James M. Slauch3, Harris Bernstein4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo 113–0032, Japan; 2: Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo 113–0032, Japan; 3: The Schoold of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL; 4: National Institutes of Health, Bethesda, MD
  • Received 03 August 2009 Accepted 12 November 2009 Published 21 October 2010
  • Address correspondence to Hajime Tokuda htokuda@morioka.u.ac.jp
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  • Abstract:

    Bacterial lipoproteins represent a unique class of membrane proteins, which are anchored to membranes through triacyl chains attached to the amino-terminal cysteine. They are involved in various functions localized in cell envelope. possesses more than 90 species of lipoproteins, most of which are localized in the outer membrane, with others being in the inner membrane. All lipoproteins are synthesized in the cytoplasm with an N-terminal signal peptide, translocated across the inner membrane by the Sec translocon to the periplasmic surface of the inner membrane, and converted to mature lipoproteins through sequential reactions catalyzed by three lipoprotein-processing enzymes: Lgt, LspA, and Lnt. The sorting of lipoproteins to the outer membrane requires a system comprising five Lol proteins. An ATP-binding cassette transporter, LolCDE, initiates the sorting by mediating the detachment of lipoproteins from the inner membrane. Formation of the LolA-lipoprotein complex is coupled to this LolCDE-dependent release reaction. LolA accommodates the amino-terminal acyl chain of lipoproteins in its hydrophobic cavity, thereby generating a hydrophilic complex that can traverse the periplasmic space by diffusion. Lipoproteins are then transferred to LolB on the outer membrane and anchored to the inner leaflet of the outer membrane by the action of LolB. In contrast, since LolCDE does not recognize lipoproteins possessing Asp at position +2, these lipoproteins remain anchored to the inner membrane. Genes for Lol proteins are widely conserved among gram-negative bacteria, and Lol-mediated outer membrane targeting of lipoproteins is considered to be the general lipoprotein localization mechanism.

  • Citation: Narita S, Tokuda H. 2010. Biogenesis and Membrane Targeting of Lipoproteins, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.7

Key Concept Ranking

Braun's lipoprotein
0.45784888
Type II Secretion System
0.39787507
Outer Membrane Proteins
0.32614926
0.45784888

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/content/journal/ecosalplus/10.1128/ecosalplus.4.3.7
2010-10-21
2017-05-28

Abstract:

Bacterial lipoproteins represent a unique class of membrane proteins, which are anchored to membranes through triacyl chains attached to the amino-terminal cysteine. They are involved in various functions localized in cell envelope. possesses more than 90 species of lipoproteins, most of which are localized in the outer membrane, with others being in the inner membrane. All lipoproteins are synthesized in the cytoplasm with an N-terminal signal peptide, translocated across the inner membrane by the Sec translocon to the periplasmic surface of the inner membrane, and converted to mature lipoproteins through sequential reactions catalyzed by three lipoprotein-processing enzymes: Lgt, LspA, and Lnt. The sorting of lipoproteins to the outer membrane requires a system comprising five Lol proteins. An ATP-binding cassette transporter, LolCDE, initiates the sorting by mediating the detachment of lipoproteins from the inner membrane. Formation of the LolA-lipoprotein complex is coupled to this LolCDE-dependent release reaction. LolA accommodates the amino-terminal acyl chain of lipoproteins in its hydrophobic cavity, thereby generating a hydrophilic complex that can traverse the periplasmic space by diffusion. Lipoproteins are then transferred to LolB on the outer membrane and anchored to the inner leaflet of the outer membrane by the action of LolB. In contrast, since LolCDE does not recognize lipoproteins possessing Asp at position +2, these lipoproteins remain anchored to the inner membrane. Genes for Lol proteins are widely conserved among gram-negative bacteria, and Lol-mediated outer membrane targeting of lipoproteins is considered to be the general lipoprotein localization mechanism.

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Figures

Image of Figure 1
Figure 1

Proteins spanning the inner membrane possess α-helical transmembrane stretches, while β-barrel proteins span the outer membrane. The outer membrane is an asymmetric lipid bilayer composed of lipopolysaccharides (LPS) in the outer leaflet and phospholipids in the inner leaflet. Many lipoproteins are anchored to the outer membrane, while some are present in the inner membrane. The major outer membrane lipoprotein, Lpp, is covalently linked to peptidoglycans in .

Citation: Narita S, Tokuda H. 2010. Biogenesis and Membrane Targeting of Lipoproteins, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.7
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Image of Figure 2
Figure 2

All lipoproteins are synthesized with an N-terminal signal peptide (green) in the cytoplasm and then translocated across the inner membrane by the Sec translocon. Lgt recognizes the consensus lipobox sequence, Leu-(Ala/Ser)-(Gly/Ala)-Cys, of prolipoproteins and forms a thioether linkage between diacylglyceryl (red) and Cys (blue) at position +1. Lipoprotein-specific signal peptidase then cleaves the signal peptide to generate apolipoproteins. Lnt transfers an acyl chain (orange) to the amino group of the N-terminal Cys, resulting in the formation of a mature lipoprotein. If the residue at position +2 (X) is Asp, lipoproteins remain in the inner membrane, while other residues cause outer membrane localization of lipoproteins.

Citation: Narita S, Tokuda H. 2010. Biogenesis and Membrane Targeting of Lipoproteins, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.7
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Image of Figure 3
Figure 3

LolCDE, LolA, and LolB each cycle between liganded and free forms. LolCDE does not recognize inner membrane-specific lipoproteins (I) with Asp at position +2. Outer membrane-specific lipoproteins bind to LolCDE. The liganded LolCDE transfers an associated lipoprotein to LolA in an ATP-dependent manner. The LolA-lipoprotein complex interacts with LolB anchored to the outer membrane, resulting in the formation of a transient LolB-lipoprotein complex. LolB targets to phospholipids and incorporates an associated lipoprotein into the outer membrane.

Citation: Narita S, Tokuda H. 2010. Biogenesis and Membrane Targeting of Lipoproteins, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.7
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