PagP crystallized from SDS/Cosolvent reveals the route for phospholipid access to the hydrocarbon ruler

Structure

Volumn 18, Issue 9, 2010, Pages 1210-1219

  Cuesta Seijo, Jose Antonio ^a   Neale, Chris ^b,c   Khan, M Adil ^d   Moktar, Joel ^d   Tran, Christopher D ^a   Bishop, Russell E ^d   Pomès, Régis ^b,c   Privé, Gilbert G ^a,c  

^a Ontario Cancer Institute and Campbell Family Cancer Research Institute   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROCARBON; MEMBRANE ENZYME; PAGPP PROTEIN; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CATALYSIS; CIRCULAR DICHROISM; CRYSTALLIZATION; ENZYME ASSAY; ESCHERICHIA COLI; MOLECULAR CLONING; MOLECULAR DYNAMICS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

ACYLTRANSFERASES; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; CIRCULAR DICHROISM; CRYSTALLOGRAPHY; ESCHERICHIA COLI PROTEINS; GLYCOLS; LIPID A; MODELS, MOLECULAR; PHOSPHOLIPIDS; PROTEIN CONFORMATION; SODIUM DODECYL SULFATE; SOLVENTS;

ESCHERICHIA COLI;

EID: 77956309034     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.06.014     Document Type: Article

References (66)

1. Ahn V.E., Lo E.I., Engel C.K., Chen L., Hwang P.M., Kay L.E., Bishop R.E., Privé G.G. A hydrocarbon ruler measures palmitate in the enzymatic acylation of endotoxin. EMBO J. 2004, 23:2931-2941.
2. Amadei A., Linssen A.B., de Groot B.L., van Aalten D.M., Berendsen H.J. An efficient method for sampling the essential subspace of proteins. J. Biomol. Struct. Dyn. 1996, 13:615-625.
3. Anand K., Pal D., Hilgenfeld R. An overview on 2-methyl-2,4-pentanediol in crystallization and in crystals of biological macromolecules. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1722-1728.
4. Arand M., Friedberg T., Oesch F. Colorimetric quantitation of trace amounts of sodium lauryl sulfate in the presence of nucleic acids and proteins. Anal. Biochem. 1992, 207:73-75.
5. Bader M.W., Sanowar S., Daley M.E., Schneider A.R., Cho U., Xu W., Klevit R.E., Le Moual H., Miller S.I. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 2005, 122:461-472.
6. Berger O., Edholm O., Jahnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 1997, 72:2002-2013.
7. Bishop R.E. The lipid A palmitoyltransferase PagP: molecular mechanisms and role in bacterial pathogenesis. Mol. Microbiol. 2005, 57:900-912.
8. Bishop R.E., Gibbons H.S., Guina T., Trent M.S., Miller S.I., Raetz C.R. Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J. 2000, 19:5071-5080.
9. Chakrabarti N., Neale C., Payandeh J., Pai E.F., Pomés R. An iris-like mechanism of pore dilation in the CorA magnesium transport system. Biophys. J. 2010, 98:784-792.
10. Cherezov V., Yamashita E., Liu W., Zhalnina M., Cramer W.A., Caffrey M. In meso structure of the cobalamin transporter, BtuB, at 1.95 A resolution. J. Mol. Biol. 2006, 364:716-734.
11. Coiro V., Mazza F. Crystal phases of dodecyl sulfates obtained from aqueous solutions: structure of the hexaaquamagnesium salt. Crystal Structure Communications 1991, 47:1169-1173.
12. Cox K., Sansom M.S. One membrane protein, two structures and six environments: a comparative molecular dynamics simulation study of the bacterial outer membrane protein PagP. Mol. Membr. Biol. 2009, 26:205-214.
13. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall W.B., Snoeyink J., Richardson J.S., Richardson D.C. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383. 10.1093/nar/gkm216.
14. DeLano, W.L. (2002). The PyMOL Molecular Graphics System.
15. Edelhoch H. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 1967, 6:1948-1954.
16. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
17. Evanics F., Hwang P.M., Cheng Y., Kay L.E., Prosser R.S. Topology of an outer-membrane enzyme: Measuring oxygen and water contacts in solution NMR studies of PagP. J. Am. Chem. Soc. 2006, 128:8256-8264.
18. Guo L., Lim K.B., Poduje C.M., Daniel M., Gunn J.S., Hackett M., Miller S.I. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 1998, 95:189-198.
19. Guo X.H., Zhao N.M., Chen S.H., Teixeira J. Small-angle neutron scattering study of the structure of protein/detergent complexes. Biopolymers 1990, 29:335-346.
20. Hearn E.M., Patel D.R., Lepore B.W., Indic M., van den Berg B. Transmembrane passage of hydrophobic compounds through a protein channel wall. Nature 2009, 458:367-370.
21. Heaslet H., Rosenfeld R., Giffin M., Lin Y.C., Tam K., Torbett B.E., Elder J.H., McRee D.E., Stout C.D. Conformational flexibility in the flap domains of ligand-free HIV protease. Acta Crystallogr. D Biol. Crystallogr. 2007, 63:866-875.
22. Helenius A., Simons K. Solubilization of membranes by detergents. Biochim. Biophys. Acta 1975, 415:29-79.
23. Huber G.A., Kim S. Weighted-ensemble Brownian dynamics simulations for protein association reactions. Biophys. J. 1996, 70:97-110.
24. Hunte C., Richers S. Lipids and membrane protein structures. Curr. Opin. Struct. Biol. 2008, 18:406-411.
25. Huysmans G.H., Radford S.E., Brockwell D.J., Baldwin S.A. The N-terminal helix is a post-assembly clamp in the bacterial outer membrane protein PagP. J. Mol. Biol. 2007, 373:529-540.
26. Huysmans G.H., Baldwin S.A., Brockwell D.J., Radford S.E. The transition state for folding of an outer membrane protein. Proc. Natl. Acad. Sci. USA 2010, 107:4099-4104.
27. Hwang P.M., Choy W.Y., Lo E.I., Chen L., Forman-Kay J.D., Raetz C.R., Privé G.G., Bishop R.E., Kay L.E. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl. Acad. Sci. USA 2002, 99:13560-13565.
28. Hwang P.M., Bishop R.E., Kay L.E. The integral membrane enzyme PagP alternates between two dynamically distinct states. Proc. Natl. Acad. Sci. USA 2004, 101:9618-9623.
29. Jia W., El Zoeiby A., Petruzziello T.N., Jayabalasingham B., Seyedirashti S., Bishop R.E. Lipid trafficking controls endotoxin acylation in outer membranes of Escherichia coli. J. Biol. Chem. 2004, 279:44966-44975.
30. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Cryst. 1976, A32:922-923.
31. Kaminski G., Friesner R., Tirado-Rives J., Jorgensen W. Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides. J. Phys. Chem. B 2001, 105:6474-6487.
32. Kawasaki K., Ernst R.K., Miller S.I. 3-O-deacylation of lipid A by PagL, a PhoP/PhoQ-regulated deacylase of Salmonella typhimurium, modulates signaling through Toll-like receptor 4. J. Biol. Chem. 2004, 279:20044-20048.
33. Khan M.A., Bishop R.E. Molecular mechanism for lateral lipid diffusion between the outer membrane external leaflet and a beta-barrel hydrocarbon ruler. Biochemistry 2009, 48:9745-9756.
34. Khan M.A., Neale C., Michaux C., Pomès R., Privé G.G., Woody R.W., Bishop R.E. Gauging a hydrocarbon ruler by an intrinsic exciton probe. Biochemistry 2007, 46:4565-4579.
35. Khan M.A., Moktar J., Mott P.J., Bishop R.E. A thiolate anion buried within the hydrocarbon ruler perturbs PagP lipid acyl chain selection. Biochemistry 2010, 49:2368-2379.
36. Kissinger C.R., Gehlhaar D.K., Fogel D.B. Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. D Biol. Crystallogr. 1999, 55:484-491.
37. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993, 26:283-291.
38. Lindahl E., Hess B., van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 2001, 7:306-317.
39. Manning M., Colon W. Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward beta-sheet structure. Biochemistry 2004, 43:11248-11254.
40. Mattice W.L., Riser J.M., Clark D.S. Conformational properties of the complexes formed by proteins and sodium dodecyl sulfate. Biochemistry 1976, 15:4264-4272.
41. Michaux C., Pomroy N.C., Privé G.G. Refolding SDS-denatured proteins by the addition of amphipathic cosolvents. J. Mol. Biol. 2008, 375:1477-1488.
42. Michaux C., Pouyez J., Wouters J., Privé G.G. Protecting role of cosolvents in protein denaturation by SDS: a structural study. BMC Struct. Biol. 2008, 8:29.
43. Minor W., Cymborowski M., Otwinowski Z., Chruszcz M. HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr. D Biol. Crystallogr. 2006, 62:859-866.
44. Muroi M., Ohnishi T., Tanamoto K. MD-2, a novel accessory molecule, is involved in species-specific actions of Salmonella lipid A. Infect. Immun. 2002, 70:3546-3550.
45. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 1997, 53:240-255.
46. Naveed H., Jackups R., Liang J. Predicting weakly stable regions, oligomerization state, and protein-protein interfaces in transmembrane domains of outer membrane proteins. Proc. Natl. Acad. Sci. USA 2009, 106:12735-12740.
47. Nielsen M.M., Andersen K.K., Westh P., Otzen D.E. Unfolding of beta-sheet proteins in SDS. Biophys. J. 2007, 92:3674-3685.
48. Otzen D.E. Protein unfolding in detergents: effect of micelle structure, ionic strength, pH, and temperature. Biophys. J. 2002, 83:2219-2230.
49. Otzen D.E., Oliveberg M. Burst-phase expansion of native protein prior to global unfolding in SDS. J. Mol. Biol. 2002, 315:1231-1240.
50. Pilione M.R., Pishko E.J., Preston A., Maskell D.J., Harvill E.T. pagP is required for resistance to antibody-mediated complement lysis during Bordetella bronchiseptica respiratory infection. Infect. Immun. 2004, 72:2837-2842.
51. Pittz E.P., Timasheff S.N. Interaction of ribonuclease A with aqueous 2-methyl-2,4-pentanediol at pH 5.8. Biochemistry 1978, 17:615-623.
52. Potterton E., Briggs P., Turkenburg M., Dodson E. A graphical user interface to the CCP4 program suite. Acta Crystallogr. D Biol. Crystallogr. 2003, 59:1131-1137.
53. Preston A., Maxim E., Toland E., Pishko E.J., Harvill E.T., Caroff M., Maskell D.J. Bordetella bronchiseptica PagP is a Bvg-regulated lipid A palmitoyl transferase that is required for persistent colonization of the mouse respiratory tract. Mol. Microbiol. 2003, 48:725-736.
54. Privé G.G. Detergents for the stabilization and crystallization of membrane proteins. Methods 2007, 41:388-397.
55. Qin L., Hiser C., Mulichak A., Garavito R.M., Ferguson-Miller S. Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase. Proc. Natl. Acad. Sci. USA 2006, 103:16117-16122.
56. Raetz C.R., Reynolds C.M., Trent M.S., Bishop R.E. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 2007, 76:295-329.
57. Raman P., Cherezov V., Caffrey M. The Membrane Protein Data Bank. Cell. Mol. Life Sci. 2006, 63:36-51.
58. Reynolds J.A., Tanford C. The gross conformation of protein-sodium dodecyl sulfate complexes. J. Biol. Chem. 1970, 245:5161-5165.
59. Robey M., O'Connell W., Cianciotto N.P. Identification of Legionella pneumophila rcp, a pagP-like gene that confers resistance to cationic antimicrobial peptides and promotes intracellular infection. Infect. Immun. 2001, 69:4276-4286.
60. Samso M., Daban J.R., Hansen S., Jones G.R. Evidence for sodium dodecyl sulfate/protein complexes adopting a necklace structure. Eur. J. Biochem. 1995, 232:818-824.
61. Smith B.J. SDS polyacrylamide gel electrophoresis of proteins. Methods Mol. Biol. 1994, 32:23-34.
62. Smith A.E., Kim S.H., Liu F., Jia W., Vinogradov E., Gyles C.L., Bishop R.E. PagP activation in the outer membrane triggers R3 core oligosaccharide truncation in the cytoplasm of Escherichia coli O157:H7. J. Biol. Chem. 2008, 283:4332-4343.
63. Snijder H.J., Van Eerde J.H., Kingma R.L., Kalk K.H., Dekker N., Egmond M.R., Dijkstra B.W. Structural investigations of the active-site mutant Asn156Ala of outer membrane phospholipase A: function of the Asn-His interaction in the catalytic triad. Protein Sci. 2001, 10:1962-1969.
64. Tanamoto K., Azumi S. Salmonella-type heptaacylated lipid A is inactive and acts as an antagonist of lipopolysaccharide action on human line cells. J. Immunol. 2000, 164:3149-3156.
65. Tieleman D.P., Forrest L.R., Sansom M.S., Berendsen H.J. Lipid properties and the orientation of aromatic residues in OmpF, influenza M2, and alamethicin systems: molecular dynamics simulations. Biochemistry 1998, 37:17554-17561.
66. Vandeputte-Rutten L., Kramer R.A., Kroon J., Dekker N., Egmond M.R., Gros P. Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J. 2001, 20:5033-5039.