Relationship between glycolipozyme MPIase and components comprising the protein transport machinery
Main Article Content
Abstract
Protein integration into and translocation across biological membranes are vital processes for living cells. The molecular mechanisms underlying these processes are conserved at a fundamental level in all organisms from bacteria to higher plants and animals. Recently, we identified a novel factor involved in protein integration and translocation in the cytoplasmic membrane of E. coli. This factor turned out to be a glycolipid consisting of a glycan chain with a repeating unit of three N-acetylated aminosugars, and diacylglycerol connected through a pyrophosphate linker. After this glycolipid was shown to catalyze protein integration, we named it MPIase (membrane protein integrase). MPIase drives protein integration by directly interacting with membrane proteins like a molecular chaperone dedicated to membrane proteins. From this function of MPIase, we proposed the concept of ‘glycolipozyme’. We also found that during protein translocation MPIase modulates the structure of SecYEG, a protein-conducting channel. Thus, MPIase possesses critical functions in both protein translocation and integration, suggesting the presence of eukaryotic MPIase homologues. Possible interaction of MPIase with components of the protein transport machinery, including SecYEG and YidC, will be discussed.
Article Details
How to Cite
NISHIYAMA, Ken-ichi; ENDO, Yuta.
Relationship between glycolipozyme MPIase and components comprising the protein transport machinery.
Medical Research Archives, [S.l.], v. 2, n. 11, dec. 2015.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/403>. Date accessed: 22 dec. 2024.
Keywords
protein translocation; protein integration; glycolipozyme; membrane protein integrase (MPIase)
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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Chang YY, Kennedy EP (1967) Pathways for the synthesis of glycerophosphatides in Escherichia coli. J Biol Chem 242: 516-519
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Blobel G, Walter P, Chang CN, Goldman BM, Erickson AH, Lingappa VR (1979) Translocation of proteins across membranes: the signal hypothesis and beyond. Symp Soc Exp Biol 33: 9-36
Breyton C, Haase W, Rapoport TA, Kuhlbrandt W, Collinson I (2002) Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418: 662-665
Bruix M, Jimenez-Barbero J, Cronet P (1995) Determination by NMR spectroscopy of the structure and conformational features of the enterobacterial common antigen isolated from Escherichia coli. Carbohydr Res 273: 157-170
Celebi N, Dalbey RE, Yuan J (2008) Mechanism and hydrophobic forces driving membrane protein insertion of subunit II of cytochrome bo 3 oxidase. J Mol Biol 375: 1282-1292
Chang YY, Kennedy EP (1967) Pathways for the synthesis of glycerophosphatides in Escherichia coli. J Biol Chem 242: 516-519
Date T, Goodman JM, Wickner WT (1980) Procoat, the precursor of M13 coat protein, requires an electrochemical potential for membrane insertion. Proc Natl Acad Sci U S A 77: 4669-4673
Ebeling W, Hennrich N, Klockow M, Metz H, Orth HD, Lang H (1974) Proteinase K from Tritirachium album Limber. Eur J Biochem 47: 91-97
Geller BL, Wickner W (1985) M13 procoat inserts into liposomes in the absence of other membrane proteins. J Biol Chem 260: 13281-13285
Geng Y, Kedrov A, Caumanns JJ, Crevenna AH, Lamb DC, Beckmann R, Driessen AJ (2015) Role of the Cytosolic Loop C2 and the C Terminus of YidC in Ribosome Binding and Insertion Activity. J Biol Chem 290: 17250-17261
Hanada M, Nishiyama KI, Mizushima S, Tokuda H (1994) Reconstitution of an efficient protein translocation machinery comprising SecA and the three membrane proteins, SecY, SecE, and SecG (p12). J Biol Chem 269: 23625-23631
Hegde RS, Keenan RJ (2011) Tail-anchored membrane protein insertion into the endoplasmic reticulum. Nat Rev Mol Cell Biol 12: 787-798
Herrmann JM, Neupert W, Stuart RA (1997) Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p. EMBO J 16: 2217-2226
Icho T (1988) Membrane-bound phosphatases in Escherichia coli: sequence of the pgpB gene and dual subcellular localization of the pgpB product. J Bacteriol 170: 5117-5124
Jackson BJ, Bohin JP, Kennedy EP (1984) Biosynthesis of membrane-derived oligosaccharides: characterization of mdoB mutants defective in phosphoglycerol transferase I activity. J Bacteriol 160: 976-981
Kaufmann A, Manting EH, Veenendaal AK, Driessen AJ, van der Does C (1999) Cysteine-directed cross-linking demonstrates that helix 3 of SecE is close to helix 2 of SecY and helix 3 of a neighboring SecE. Biochemistry 38: 9115-9125
Kawashima Y, Miyazaki E, Muller M, Tokuda H, Nishiyama K (2008) Diacylglycerol specifically blocks spontaneous integration of membrane proteins and allows detection of a factor-assisted integration. J Biol Chem 283: 24489-24496
Kiefer D, Hu X, Dalbey R, Kuhn A (1997) Negatively charged amino acid residues play an active role in orienting the Sec-independent Pf3 coat protein in the Escherichia coli inner membrane. EMBO J 16: 2197-2204
Kiefer D, Kuhn A (1999) Hydrophobic forces drive spontaneous membrane insertion of the bacteriophage Pf3 coat protein without topological control. EMBO J 18: 6299-6306
Koch HG, Hengelage T, Neumann-Haefelin C, MacFarlane J, Hoffschulte HK, Schimz KL, Mechler B, Muller M (1999) In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol Biol Cell 10: 2163-2173
Koch HG, Moser M, Muller M (2003) Signal recognition particle-dependent protein targeting, universal to all kingdoms of life. Rev Physiol Biochem Pharmacol 146: 55-94
Koch HG, Muller M (2000) Dissecting the translocase and integrase functions of the Escherichia coli SecYEG translocon. J Cell Biol 150: 689-694
Kol S, Turrell BR, de Keyzer J, van der Laan M, Nouwen N, Driessen AJ (2006) YidC-mediated membrane insertion of assembly mutants of subunit c of the F1F0 ATPase. J Biol Chem 281: 29762-29768
Kuhn A (1995) Major coat proteins of bacteriophage Pf3 and M13 as model systems for Sec-independent protein transport. FEMS Microbiol Rev 17: 185-190
Kuhn HM, Meier-Dieter U, Mayer H (1988) ECA, the enterobacterial common antigen. FEMS Microbiol Rev 4: 195-222
Kumazaki K, Chiba S, Takemoto M, Furukawa A, Nishiyama K, Sugano Y, Mori T, Dohmae N, Hirata K, Nakada-Nakura Y, Maturana AD, Tanaka Y, Mori H, Sugita Y, Arisaka F, Ito K, Ishitani R, Tsukazaki T, Nureki O (2014a) Structural basis of Sec-independent membrane protein insertion by YidC. Nature 509: 516-520
Kumazaki K, Kishimoto T, Furukawa A, Mori H, Tanaka Y, Dohmae N, Ishitani R, Tsukazaki T, Nureki O (2014b) Crystal structure of Escherichia coli YidC, a membrane protein chaperone and insertase. Sci Rep 4: 7299
Kuruma Y, Nishiyama K, Shimizu Y, Muller M, Ueda T (2005) Development of a minimal cell-free translation system for the synthesis of presecretory and integral membrane proteins. Biotechnol Prog 21: 1243-1251
Luirink J, von Heijne G, Houben E, de Gier JW (2005) Biogenesis of inner membrane proteins in Escherichia coli. Annu Rev Microbiol 59: 329-355
Macfarlane J, Muller M (1995) The functional integration of a polytopic membrane protein of Escherichia coli is dependent on the bacterial signal-recognition particle. Eur J Biochem 233: 766-771
Moore M, Harrison MS, Peterson EC, Henry R (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275: 1529-1532
Moser M, Nagamori S, Huber M, Tokuda H, Nishiyama K (2013) Glycolipozyme MPIase is essential for topology inversion of SecG during preprotein translocation. Proc Natl Acad Sci U S A 110: 9734-9739
Nagamori S, Nishiyama K, Tokuda H (2000) Two SecG molecules present in a single protein translocation machinery are functional even after crosslinking. J Biochem 128: 129-137
Nagamori S, Nishiyama K, Tokuda H (2002) Membrane topology inversion of SecG detected by labeling with a membrane-impermeable sulfhydryl reagent that causes a close association of SecG with SecA. J Biochem 132: 629-634
Nagamori S, Smirnova IN, Kaback HR (2004) Role of YidC in folding of polytopic membrane proteins. J Cell Biol 165: 53-62
Nishiyama K, Hanada M, Tokuda H (1994) Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J 13: 3272-3277
Nishiyama K, Ikegami A, Moser M, Schiltz E, Tokuda H, Muller M (2006) A derivative of lipid A is involved in signal recognition particle/SecYEG-dependent and -independent membrane integrations. J Biol Chem 281: 35667-35676
Nishiyama K, Maeda M, Abe M, Kanamori T, Shimamoto K, Kusumoto S, Ueda T, Tokuda H (2010) A novel complete reconstitution system for membrane integration of the simplest membrane protein. Biochem Biophys Res Commun 394: 733-736
Nishiyama K, Maeda M, Yanagisawa K, Nagase R, Komura H, Iwashita T, Yamagaki T, Kusumoto S, Tokuda H, Shimamoto K (2012) MPIase is a glycolipozyme essential for membrane protein integration. Nat Commun 3: 1260
Nishiyama K, Mizushima S, Tokuda H (1993) A novel membrane protein involved in protein translocation across the cytoplasmic membrane of Escherichia coli. EMBO J 12: 3409-3415
Nishiyama K, Shimamoto K (2014) Glycolipozyme membrane protein integrase (MPIase): recent data. Biomol Concepts 5: 429-438
Nishiyama K, Suzuki T, Tokuda H (1996) Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell 85: 71-81
Raetz CR, Newman KF (1978) Neutral lipid accumulation in the membranes of Escherichia coli mutants lacking diglyceride kinase. J Biol Chem 253: 3882-3887
Rapoport TA, Goder V, Heinrich SU, Matlack KE (2004) Membrane-protein integration and the role of the translocation channel. Trends Cell Biol 14: 568-575
Reynolds CM, Kalb SR, Cotter RJ, Raetz CR (2005) A phosphoethanolamine transferase specific for the outer 3-deoxy-D-manno-octulosonic acid residue of Escherichia coli lipopolysaccharide. Identification of the eptB gene and Ca2+ hypersensitivity of an eptB deletion mutant. J Biol Chem 280: 21202-21211
Rick PD, Silver RP (1996) Enterobacterial Common Antigen and Capsular Polysaccharides In Escherichia coli and Salmonella, Cellular and Molecular Biology, 2nd edition, Neidhardt FC (ed), Vol. 1, pp 104-122. Washington, DC ASM Press
Ridder AN, Kuhn A, Killian JA, de Kruijff B (2001) Anionic lipids stimulate Sec-independent insertion of a membrane protein lacking charged amino acid side chains. EMBO Rep 2: 403-408
Robinson PJ, Woolhead CA (2013) Post-translational membrane insertion of an endogenous YidC substrate. Biochim Biophys Acta 1833: 2781-2788
Rotering H, Raetz CR (1983) Appearance of monoglyceride and triglyceride in the cell envelope of Escherichia coli mutants defective in diglyceride kinase. J Biol Chem 258: 8068-8073
Samuelson JC, Chen M, Jiang F, Moller I, Wiedmann M, Kuhn A, Phillips GJ, Dalbey RE (2000) YidC mediates membrane protein insertion in bacteria. Nature 406: 637-641
Samuelson JC, Jiang F, Yi L, Chen M, de Gier JW, Kuhn A, Dalbey RE (2001) Function of YidC for the insertion of M13 procoat protein in Escherichia coli: translocation of mutants that show differences in their membrane potential dependence and Sec requirement. J Biol Chem 276: 34847-34852
Scotti PA, Urbanus ML, Brunner J, de Gier JW, von Heijne G, van der Does C, Driessen AJ, Oudega B, Luirink J (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J 19: 542-549
Serek J, Bauer-Manz G, Struhalla G, van den Berg L, Kiefer D, Dalbey R, Kuhn A (2004) Escherichia coli YidC is a membrane insertase for Sec-independent proteins. EMBO J 23: 294-301
Stiegler N, Dalbey RE, Kuhn A (2011) M13 procoat protein insertion into YidC and SecYEG proteoliposomes and liposomes. J Mol Biol 406: 362-370
Sugai R, Takemae K, Tokuda H, Nishiyama K (2007) Topology inversion of SecG is essential for cytosolic SecA-dependent stimulation of protein translocation. J Biol Chem 282: 29540-29548
Suzuki H, Nishiyama K, Tokuda H (1998) Coupled structure changes of SecA and SecG revealed by the synthetic lethality of the secAcsR11 and delta secG::kan double mutant. Mol Microbiol 29: 331-341
Szyrach G, Ott M, Bonnefoy N, Neupert W, Herrmann JM (2003) Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria. EMBO J 22: 6448-6457
Tsukazaki T, Mori H, Fukai S, Ishitani R, Mori T, Dohmae N, Perederina A, Sugita Y, Vassylyev DG, Ito K, Nureki O (2008) Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455: 988-991
Ueda Y, Ishitsuka R, Hullin-Matsuda F, Kobayashi T (2014) Regulation of the transbilayer movement of diacylglycerol in the plasma membrane. Biochimie 107 Pt A: 43-50
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