Membrane remodeling capacity of a vesicle-inducing glycosyltransferase

FEBS Journal

Volumn 281, Issue 16, 2014, Pages 3667-3684

  Ge, Changrong ^a,b,c   Gõmez Llobregat, Jordi ^a   Skwark, Marcin J ^a,d   Ruysschaert, Jean Marie ^b   Wieslander, Åke ^a   Lindén, Martin ^a,e  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c KAROLINSKA INSTITUTE   (Sweden)

^d AALTO UNIVERSITY   (Finland)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

glycosyltransferase; lipid protein interactions; membrane deformation; molecular dynamics; monotopic protein

Indexed keywords

MONOGLUCOSYLDIACYLGLYCEROL SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG;

ACHOLEPLASMA LAIDLAWII; AMINO TERMINAL SEQUENCE; ARTICLE; BIOCHEMISTRY; BIOINFORMATICS; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE BIOLOGY; MEMBRANE REMODELING; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; SIMULATION;

ACHOLEPLASMA LAIDLAWII; ESCHERICHIA COLI; EUKARYOTA; NEGIBACTERIA;

GLYCOSYLTRANSFERASE; LIPID-PROTEIN INTERACTIONS; MEMBRANE DEFORMATION; MOLECULAR DYNAMICS; MONOTOPIC PROTEIN;

ACHOLEPLASMA LAIDLAWII; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; CELL MEMBRANE; CYTOPLASMIC VESICLES; ESCHERICHIA COLI; GLYCOSYLTRANSFERASES; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84906790511     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12889     Document Type: Article

References (71)

1. Bernsel A, &, Daley DO, (2009) Exploring the inner membrane proteome of Escherichia coli: which proteins are eluding detection and why? Trends Microbiol 17, 444-449.
2. Papanastasiou M, Orfanoudaki G, Koukaki M, Kountourakis N, Sardis MF, Aivaliotis M, Karamanou S, &, Economou A, (2013) The Escherichia coli peripheral inner membrane proteome. Mol Cell Proteomics 12, 599-610.
3. Forneris F, &, Mattevi A, (2008) Enzymes without borders: mobilizing substrates, delivering products. Science 321, 213-216.
4. Nichols FC, Bajrami B, Clark RB, Housley W, &, Yao X, (2012) Free lipid A isolated from Porphyromonas gingivalis lipopolysaccharide is contaminated with phosphorylated dihydroceramide lipids: recovery in diseased dental samples. Infect Immun 80, 860-874.
5. Pei B, Vela JL, Zajonc D, &, Kronenberg M, (2012) Interplay between carbohydrate and lipid in recognition of glycolipid antigens by natural killer T cells. Ann N Y Acad Sci 1253, 68-79.
6. Reichmann NT, &, Gründling A, (2011) Location, synthesis and function of glycolipids and polyglycerolphosphate lipoteichoic acid in Gram-positive bacteria of the phylum Firmicutes. FEMS Microbiol Lett 319, 97-105.
7. Lairson LL, Henrissat B, Davies GJ, &, Withers SG, (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77, 521-555.
8. Berg S, Edman M, Li L, Wikström M, &, Wieslander Å, (2001) Sequence properties of the 1,2-diacylglycerol 3-glucosyltransferase from Acholeplasma laidlawii membranes. Recognition of a large group of lipid glycosyltransferases in eubacteria and archaea. J Biol Chem 276, 22056-22063.
9. Dahlqvist A, Nordström S, Karlsson OP, Mannock DA, McElhaney RN, &, Wieslander Å, (1995) Efficient modulation of glucolipid enzyme activities in membranes of Acholeplasma laidlawii by the type of lipids in the bilayer matrix. Biochemistry 34, 13381-13389.
10. Hölzl G, &, Dörmann P, (2007) Structure and function of glycoglycerolipids in plants and bacteria. Prog Lipid Res 46, 225-243.
11. Theilacker C, Sanchez-Carballo P, Toma I, Fabretti F, Sava I, Kropec A, Holst O, &, Huebner J, (2009) Glycolipids are involved in biofilm accumulation and prolonged bacteraemia in Enterococcus faecalis. Mol Microbiol 71, 1055-1069.
12. Webb AJ, Karatsa-Dodgson M, &, Gründling A, (2009) Two-enzyme systems for glycolipid and polyglycerolphosphate lipoteichoic acid synthesis in Listeria monocytogenes. Mol Microbiol 74, 299-314.
13. Hossain H, Wellensiek HJ, Geyer R, &, Lochnit G, (2001) Structural analysis of glycolipids from Borrelia burgdorferi. Biochimie 83, 683-692.
14. Karlsson OP, Dahlqvist A, Vikström S, &, Wieslander Å, (1997) Lipid dependence and basic kinetics of the purified 1,2-diacylglycerol 3-glucosyltransferase from membranes of Acholeplasma laidlawii. J Biol Chem 272, 929-936.
15. Li L, Storm P, Karlsson OP, Berg S, &, Wieslander Å, (2003) Irreversible binding and activity control of the 1,2-diacylglycerol 3-glucosyltransferase from Acholeplasma laidlawii at an anionic lipid bilayer surface. Biochemistry 42, 9677-9686.
16. Lind J, Rämö T, Klement MLR, Bárány-Wallje E, Epand RM, Epand RF, Mäler L, &, Wieslander Å, (2007) High cationic charge and bilayer interface-binding helices in a regulatory lipid glycosyltransferase. Biochemistry 46, 5664-5677.
17. Eriksson HM, Wessman P, Ge C, Edwards K, &, Wieslander Å, (2009) Massive formation of intracellular membrane vesicles in Escherichia coli by a monotopic membrane-bound lipid glycosyltransferase. J Biol Chem 284, 33904-33914.
18. Eriksson HM, Persson K, Zhang S, &, Wieslander Å, (2009) High-yield expression and purification of a monotopic membrane glycosyltransferase. Protein Expr Purif 66, 143-148.
19. Van den Brink-van der Laan E, Boots J-WP, Spelbrink REJ, Kool GM, Breukink E, Killian JA, &, de Kruijff B, (2003) Membrane interaction of the glycosyltransferase MurG: a special role for cardiolipin. J Bacteriol 185, 3773-3779.
20. Metzger LE IV, &, Raetz CRH, (2009) Purification and characterization of the lipid A disaccharide synthase (LpxB) from Escherichia coli, a peripheral membrane protein. Biochemistry 48, 11559-11571.
21. Reynwar BJ, Illya G, Harmandaris VA, Müller MM, Kremer K, &, Deserno M, (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447, 461-464.
22. Ariöz C, Ye W, Bakali A, Ge C, Liebau J, Götzke H, Barth A, Wieslander Å, &, Mäler L, (2013) Anionic lipid binding to the foreign protein MGS provides a tight coupling between phospholipid synthesis and protein overexpression in Escherichia coli. Biochemistry 52, 5533-5544.
23. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY, Sherman MB, Geissler PL, Fletcher DA, &, Hayden CC, (2012) Membrane bending by protein-protein crowding. Nat Cell Biol 14, 944-949.
24. Skwark MJ, &, Elofsson A, (2013) PconsD: ultrarapid, accurate model quality assessment for protein structure prediction. Bioinformatics 29, 1817-1818.
25. Larsson P, Skwark MJ, Wallner B, &, Elofsson A, (2009) Assessment of global and local model quality in CASP8 using Pcons and ProQ. Proteins 77 (Suppl 9), 167-172.
26. Larsson P, Skwark MJ, Wallner B, &, Elofsson A, (2011) Improved predictions by Pcons.net using multiple templates. Bioinformatics 27, 426-427.
27. Li L, Karlsson OP, &, Wieslander Å, (1997) Activating amphiphiles cause a conformational change of the 1,2-diacylglycerol 3-glucosyltransferase from Acholeplasma laidlawii membranes according to proteolytic digestion. J Biol Chem 272, 29602-29606.
28. Szpryngiel S, Ge C, Iakovleva I, Georgiev A, Lind J, Wieslander Å, &, Mäler L, (2011) Lipid interacting regions in phosphate stress glycosyltransferase atDGD2 from Arabidopsis thaliana. Biochemistry 50, 4451-4466.
29. Ge C, Georgiev A, Öhman A, Wieslander Å, &, Kelly AA, (2011) Tryptophan residues promote membrane association for a plant lipid glycosyltransferase involved in phosphate stress. J Biol Chem 286, 6669-6684.
30. Balali-Mood K, Bond PJ, &, Sansom MSP, (2009) Interaction of monotopic membrane enzymes with a lipid bilayer: a coarse-grained MD simulation study. Biochemistry 48, 2135-2145.
31. Deplazes E, Louhivuori M, Jayatilaka D, Marrink SJ, &, Corry B, (2012) Structural investigation of MscL gating using experimental data and coarse grained MD simulations. PLoS Comput Biol 8, e1002683.
32. Arnarez C, Marrink SJ, &, Periole X, (2013) Identification of cardiolipin binding sites on cytochrome c oxidase at the entrance of proton channels. Sci Rep 3, 1263.
33. Ingõlfsson HI, Lopez CA, Uusitalo JJ, de Jong DH, Gopal SM, Periole X, &, Marrink SJ, (2014) The power of coarse graining in biomolecular simulations. Wiley Interdiscip Rev Comput Mol Sci 4, 225-248.
34. Schmidt H, Hansen G, Singh S, Hanuszkiewicz A, Lindner B, Fukase K, Woodard RW, Holst O, Hilgenfeld R, Mamat U, et al,. (2012) Structural and mechanistic analysis of the membrane-embedded glycosyltransferase WaaA required for lipopolysaccharide synthesis. Proc Natl Acad Sci USA 109, 6253-6258.
35. Guerin ME, Schaeffer F, Chaffotte A, Gest P, Giganti D, Korduláková J, van der Woerd M, Jackson M, &, Alzari PM, (2009) Substrate-induced conformational changes in the essential peripheral membrane-associated mannosyltransferase PimA from mycobacteria: implications for catalysis. J Biol Chem 284, 21613-21625.
36. Giganti DO, Alegre-Cebollada J, Urresti S, Albesa-Jove D, Rodrigo-Unzueta A, Comino N, Kachala M, Lopez-Fernandez S, Svergun DI, Fernandez JM, et al,. (2013) Conformational plasticity of the essential membrane-associated mannosyltransferase PimA from mycobacteria. J Biol Chem 288, 29797-29808.
37. Marquardt DW, (1963) An algorithm for least-squares estimation of nonlinear parameters. J Soc Ind Appl Math 11, 431-441.
38. Hunte C, (2005) Specific protein-lipid interactions in membrane proteins. Biochem Soc Trans 33, 938-942.
39. Schlattner U, Gehring F, Vernoux N, Tokarska-Schlattner M, Neumann D, Marcillat O, Vial C, &, Wallimann T, (2004) C-terminal lysines determine phospholipid interaction of sarcomeric mitochondrial creatine kinase. J Biol Chem 279, 24334-24342.
40. Schlegel S, Löfblom J, Lee C, Hjelm A, Klepsch M, Strous M, Drew D, Slotboom DJ, &, de Gier J-W, (2012) Optimizing membrane protein overexpression in the Escherichia coli strain Lemo21(DE3). J Mol Biol 423, 648-659.
41. Zhao Y, He W, Liu W-F, Liu C-C, Feng L-K, Sun L, Yan Y-B, &, Hang H-Y, (2012) Two distinct states of Escherichia coli cells that overexpress recombinant heterogeneous β-galactosidase. J Biol Chem 287, 9259-9268.
42. Albesa-Jove D, Giganti D, Jackson M, Alzari PM, &, Guerin ME, (2013) Structure-function relationships of membrane-associated GT-B glycosyltransferases. Glycobiology 24, 108-124.
43. Ahn VE, Faull KF, Whitelegge JP, Fluharty AL, &, Privé GG, (2003) Crystal structure of saposin B reveals a dimeric shell for lipid binding. Proc Natl Acad Sci USA 100, 38-43.
44. Boal DH, (2012) Mechanics of the Cell. Cambridge University Press, Cambridge.
45. Carnahan NF, &, Starling KE, (1969) Equation of state for non-attracting rigid spheres. J Chem Phys 51, 635-636.
46. Song Y, Mason EA, &, Stratt RM, (1989) Why does the Carnahan-Starling equation work so well? J Phys Chem 93, 6916-6919.
47. Minton AP, (2000) Effects of excluded surface area and adsorbate clustering on surface adsorption of proteins I. Equilibrium models. Biophys Chem 86, 239-247.
48. Lindén M, Sens P, &, Phillips R, (2012) Entropic tension in crowded membranes. PLoS Comput Biol 8, e1002431.
49. Baumgart T, Capraro BR, Zhu C, &, Das SL, (2011) Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu Rev Phys Chem 62, 483-506.
50. Ramesh P, Baroji YF, Reihani SNS, Stamou D, Oddershede LB, &, Bendix PM, (2013) FBAR syndapin 1 recognizes and stabilizes highly curved tubular membranes in a concentration dependent manner. Sci Rep 3, 1565.
51. Shevchenko A, Wilm M, Vorm O, &, Mann M, (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68, 850-858.
52. Buser CA, &, McLaughlin S, (1998) Ultracentrifugation technique for measuring the binding of peptides and proteins to sucrose-loaded phospholipid vesicles. In Transmembrane Signaling Protocols (, Bar-Sagi D, ed), Meth Mol Biol 84, 267-282. Humana Press, Totowa, NJ, USA.
53. Soding J, Biegert A, &, Lupas AN, (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33, W244-W248.
54. Söding J, (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21, 951-960.
55. Ray A, Lindahl E, &, Wallner B, (2012) Improved model quality assessment using ProQ2. BMC Bioinformatics 13, 224.
56. Raman S, Vernon R, Thompson J, Tyka M, Sadreyev R, Pei J, Kim D, Kellogg E, DiMaio F, Lange O, et al,. (2009) Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins 77 (Suppl 9), 89-99.
57. Yang Y, &, Zhou Y, (2008) Specific interactions for ab initio folding of protein terminal regions with secondary structures. Proteins 72, 793-803.
58. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, &, Richardson DC, (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66, 12-21.
59. Hess B, Kutzner C, van der Spoel D, &, Lindahl E, (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4, 435-447.
60. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, &, de Vries AH, (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B 111, 7812-7824.
61. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, &, Marrink SJ, (2008) The MARTINI coarse-grained force field: extension to proteins. J Chem Theory Comput 4, 819-834.
62. Atilgan AR, Durell SR, Jernigan RL, Demirel MC, Keskin O, &, Bahar I, (2001) Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys J 80, 505-515.
63. Miyamoto S, &, Kollman PA, (1992) SETTLE: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 13, 952-962.
64. Bussi G, Donadio D, &, Parrinello M, (2007) Canonical sampling through velocity rescaling. J Chem Phys 126, 014101.
65. Yesylevskyy SO, Schäfer LV, Sengupta D, &, Marrink SJ, (2010) Polarizable water model for the coarse-grained MARTINI force field. PLoS Comput Biol 6, e1000810.
66. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, &, Pedersen LG, (1995) A smooth particle mesh Ewald method. J Chem Phys 103, 8577-8593.
67. Marrink SJ, de Vries AH, &, Mark AE, (2004) Coarse grained model for semiquantitative lipid simulations. J Phys Chem B 108, 750-760.
68. Baoukina S, Monticelli L, Amrein M, &, Tieleman DP, (2007) The molecular mechanism of monolayer-bilayer transformations of lung surfactant from molecular dynamics simulations. Biophys J 93, 3775-3782.
69. Dahlberg M, &, Maliniak A, (2010) Mechanical properties of coarse-grained bilayers formed by cardiolipin and zwitterionic lipids. J Chem Theory Comput 6, 1638-1649.
70. Snider C, Jayasinghe S, Hristova K, &, White SH, (2009) MPEx: a tool for exploring membrane proteins. Protein Sci 18, 2624-2628.
71. Eisenberg D, Weiss RM, Terwilliger TC, &, Wilcox W, (1982) Hydrophobic moments and protein structure. Faraday Symp Chem Soc 17, 109-120.