LptE binds to and alters the physical state of LPS to catalyze its assembly at the cell surface

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 26, 2014, Pages 9467-9472

  Malojčić, Goran ^a   Andres, Dorothee ^a   Grabowicz, Marcin ^b   George, Alexander H ^a   Ruiz, Natividad ^c   Silhavy, Thomas J ^b   Kahne, Daniel ^a,d  

^a HARVARD UNIVERSITY   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Endotoxin; Glycolipid binding; Membrane asymmetry; Membrane biogenesis; Vesicles

Indexed keywords

CARRIER PROTEIN; ESCHERICHIA COLI PROTEIN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; LIPOPROTEIN; LIPOPROTEIN LPTE; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BIOGENESIS; CATALYSIS; CELL SURFACE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTRON MICROSCOPY; ESCHERICHIA COLI; NONHUMAN; PHYSICAL CHEMISTRY; POINT MUTATION; PRIORITY JOURNAL; WILD TYPE;

ENDOTOXIN; GLYCOLIPID BINDING; MEMBRANE ASYMMETRY; MEMBRANE BIOGENESIS; VESICLES;

BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; CATALYSIS; CRYSTALLIZATION; ESCHERICHIA COLI PROTEINS; LIPOPOLYSACCHARIDES; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES;

EID: 84903689545     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1402746111     Document Type: Article

References (49)

1. Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700.
2. Muhlradt PF, Golecki JR (1975) Asymmetrical distribution and artifactual reorientation of lipopolysaccharide in the outer membrane bilayer of Salmonella typhimurium. FEBS 51(2):343-352.
3. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67(4):593-656.
4. Chng SS, Gronenberg LS, Kahne D (2010) Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49(22): 4565-4567.
5. Sperandeo P, et al. (2008) Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190(13):4460-4469.
6. Sperandeo P, Pozzi C, Dehò G, Polissi A (2006) Non-essential KDO biosynthesis and new essential cell envelope biogenesis genes in the Escherichia coli yrbG-yhbG locus. Res Microbiol 157(6):547-558.
7. Tran AX, Dong C, Whitfield C (2010) Structure and functional analysis of LptC, a conserved membrane protein involved in the lipopolysaccharide export pathway in Escherichia coli. J Biol Chem 285(43):33529-33539.
8. Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ (2008) Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 105(14):5537-5542.
9. Okuda S, Freinkman E, Kahne D (2012) Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338(6111):1214-1217.
10. Suits MD, Sperandeo P, Dehò G, Polissi A, Jia Z (2008) Novel structure of the conserved gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J Mol Biol 380(3):476-488.
11. Chng SS, Ruiz N, Chimalakonda G, Silhavy TJ, Kahne D (2010) Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc Natl Acad Sci USA 107(12):5363-5368.
12. Wu T, et al. (2006) Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103(31): 11754-11759.
13. Nikaido H, Vaara M (1985) Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49(1):1-32.
14. Nikaido H (1988) Structure and functions of the cell envelope of gram-negative bacteria. Rev Infect Dis 10(Suppl 2):S279-S281.
15. Freinkman E, Chng SS, Kahne D (2011) The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc Natl Acad Sci USA 108(6):2486-2491.
16. Chimalakonda G, et al. (2011) Lipoprotein LptE is required for the assembly of LptD by the beta-barrel assembly machine in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 108(6):2492-2497.
17. Chng SS, et al. (2012) Disulfide rearrangement triggered by translocon assembly controls lipopolysaccharide export. Science 337(6102):1665-1668.
18. Ruiz N, Chng SS, Hiniker A, Kahne D, Silhavy TJ (2010) Nonconsecutive disulfide bond formation in an essential integral outer membrane protein. Proc Natl Acad Sci USA 107(27):12245-12250.
19. Bos MP, Tommassen J (2011) The LptD chaperone LptE is not directly involved in lipopolysaccharide transport in Neisseria meningitidis. J Biol Chem 286(33):28688-28696.
20. Chimalakonda G (2011) Lipopolysaccharide transport in Escherichia coli. PhD thesis (Princeton Univ, Princeton) .
21. Evans DG, Evans DJ, Jr., Moulds JJ, Graham DY (1988) N- acetylneuraminyllactosebinding fibrillar hemagglutinin of Campylobacter pylori: A putative colonization factor antigen. Infect Immun 56(11):2896-2906.
22. Moran AP, Prendergast MM, Appelmelk BJ (1996) Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol Med Microbiol 16(2):105-115.
23. Hoess A, Watson S, Siber GR, Liddington R (1993) Crystal structure of an endotoxinneutralizing protein from the horseshoe crab, Limulus anti-LPS factor, at 1.5 A resolution. EMBO J 12(9):3351-3356.
24. Morita T, et al. (1985) Isolation and biological activities of limulus anticoagulant (anti-LPS factor) which interacts with lipopolysaccharide (LPS) . J Biochem 97(6):1611-1620.
25. Nachum R, Watson SW, Sullivan JD, Jr., Siegel SE (1979) Antimicrobial defense mechanisms in the horseshoe crab, Limulus polyphemus: Preliminary observations with heat-derived extracts of Limulus amoebocyte lysate. J Invertebr Pathol 33(3): 290-299.
26. Ferguson AD, et al. (2000) A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure 8(6):585-592.
27. Ried C, et al. (1996) High affinity endotoxin-binding and neutralizing peptides based on the crystal structure of recombinant Limulus anti-lipopolysaccharide factor. J Biol Chem 271(45):28120-28127.
28. Ruiz N, Falcone B, Kahne D, Silhavy TJ (2005) Chemical conditionality: A genetic strategy to probe organelle assembly. Cell 121(2):307-317.
29. Wu T, et al. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121(2):235-245.
30. Ruiz N, Wu T, Kahne D, Silhavy TJ (2006) Probing the barrier function of the outer membrane with chemical conditionality. ACS Chem Biol 1(6):385-395.
31. Grabowicz M, Yeh J, Silhavy TJ (2013) Dominant negative lptE mutation that supports a role for LptE as a plug in the LptD barrel. J Bacteriol 195(6):1327-1334.
32. Richter W, et al. (2011) Morphology, size distribution, and aggregate structure of lipopolysaccharide and lipid A dispersions from enterobacterial origin. Innate Immunity 17(5):427-438.
33. Andrä J, et al. (2008) Surface acoustic wave biosensor as a tool to study the interaction of antimicrobial peptides with phospholipid and lipopolysaccharide model membranes. Langmuir 24(16):9148-9153.
34. Danner RL, et al. (1989) Purification, toxicity, and antiendotoxin activity of polymyxin B nonapeptide. Antimicrob Agents Chemother 33(9):1428-1434.
35. Andra J, et al. (2004) Biophysical characterization of the interaction of Limulus polyphemus endotoxin neutralizing protein with lipopolysaccharide. FEBS 271(10): 2037-2046.
36. Devleeschouwer MJ, Cornil MF, Dony J (1985) Studies on the sensitivity and specificity of the Limulus amebocyte lysate test and rabbit pyrogen assays. Appl Environ Microbiol 50(6):1509-1511.
37. Bayer ME (1991) Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. J Struct Biol 107(3):268-280.
38. Gutsmann T, et al. (2005) Lipid-mediated resistance of Gram-negative bacteria against various pore-forming antimicrobial peptides. J Endotoxin Res 11(3):167-173.
39. Gutsmann T, et al. (2000) Lipopolysaccharide-binding protein-mediated interaction of lipid A from different origin with phospholipid membranes. Phys Chem Chem Phys 2(20):4521-4528.
40. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W (1998) Siderophoremediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide. Science 282(5397):2215-2220.
41. Beamer LJ, Carroll SF, Eisenberg D (1997) Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution. Science 276(5320):1861-1864.
42. Eckert JK, et al. (2013) The crystal structure of lipopolysaccharide binding protein reveals the location of a frequent mutation that impairs innate immunity. Immunity 39(4):647-660.
43. Weiss J (2003) Bactericidal/permeability-increasing protein (BPI) and lipopolysaccharide-binding protein (LBP): Structure, function and regulation in host defence against Gram-negative bacteria. Biochem Soc Trans 31(Pt 4):785-790.
44. Schromm AB, et al. (1996) Lipopolysaccharide-binding protein mediates CD14-independent intercalation of lipopolysaccharide into phospholipid membranes. FEBS Lett 399(3):267-271.
45. Ohvo-Rekilä H, Mattjus P (2011) Monitoring glycolipid transfer protein activity and membrane interaction with the surface plasmon resonance technique. Biochim Biophys Acta 1808(1):47-54.
46. Sugiki T, Takahashi H, Nagasu M, Hanada K, Shimada I (2010) Real-time assay method of lipid extraction activity. Anal Biochem 399(2):162-167.
47. Rypniewski WR, Holden HM, Rayment I (1993) Structural consequences of reductive methylation of lysine residues in hen egg white lysozyme: An X-ray analysis at 1.8-A resolution. Biochemistry 32(37):9851-9858.
48. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229(1):105-124.
49. Malojcic G, et al. (2008) A structural and biochemical basis for PAPS-independent sulfuryl transfer by aryl sulfotransferase from uropathogenic Escherichia coli. Proc Natl Acad Sci USA 105(49):19217-19222.