1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Microbiology
  4. Volume 70, 2016
  5. Article

Annual Review of Microbiology

Volume 70, 2016

The Power of Asymmetry: Architecture and Assembly of the Gram-Negative Outer Membrane Lipid Bilayer

Abstract

Determining the chemical composition of biological materials is paramount to the study of natural phenomena. Here, we describe the composition of model gram-negative outer membranes, focusing on the predominant assembly, an asymmetrical bilayer of lipid molecules. We also give an overview of lipid biosynthetic pathways and molecular mechanisms that organize this material into the outer membrane bilayer. An emphasis is placed on the potential of these pathways as targets for antibiotic development. We discuss deviations in composition, through bacterial cell surface remodeling, and alternative modalities to the asymmetric lipid bilayer. Outer membrane lipid alterations of current microbiological interest, such as lipid structures found in commensal bacteria, are emphasized. Additionally, outer membrane components could potentially be engineered to develop vaccine platforms. Observations related to composition and assembly of gram-negative outer membranes will continue to generate novel discoveries, broaden biotechnologies, and reveal profound mysteries to compel future research.

Keyword(s): commensals, lipid A, lipopolysaccharide, LPS, outer membrane vesicles, phospholipids, vaccines
Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-102215-095308
2016-09-08
2025-04-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/70/1/annurev-micro-102215-095308.html?itemId=/content/journals/10.1146/annurev-micro-102215-095308&mimeType=html&fmt=ahah

Literature Cited

  1. Acevedo R, Fernández S, Zayas C, Acosta A, Sarmiento ME. 1.  et al. 2014. Bacterial outer membrane vesicles and vaccine applications. Front. Immunol. 5:121 [Google Scholar]
  2. Anderson MS, Robertson AD, Macher I, Raetz CR. 2.  1988. Biosynthesis of lipid A in Escherichia coli: Identification of UDP-3-O-[(R)-3-hydroxymyristoyl]-α-d-glucosamine as a precursor of UDP-N2,O3-bis[(R)-3-hydroxymyristoyl]-α-d-glucosamine. Biochemistry 27:61908–17 [Google Scholar]
  3. Asensio CJA, Gaillard ME, Moreno G, Bottero D, Zurita E. 3.  et al. 2011. Outer membrane vesicles obtained from Bordetella pertussis Tohama expressing the lipid A deacylase PagL as a novel acellular vaccine candidate. Vaccine 29:81649–56 [Google Scholar]
  4. Bainbridge BW, Karimi-Naser L, Reife R, Blethen F, Ernst RK, Darveau RP. 4.  2008. Acyl chain specificity of the acyltransferases LpxA and LpxD and substrate availability contribute to lipid A fatty acid heterogeneity in Porphyromonas gingivalis. J. Bacteriol. 190:134549–58 [Google Scholar]
  5. Barb AW, McClerren AL, Snehelatha K, Reynolds CM, Zhou P, Raetz CRH. 5.  2007. Inhibition of lipid A biosynthesis as the primary mechanism of CHIR-090 antibiotic activity in Escherichia coli. Biochemistry 46:123793–802 [Google Scholar]
  6. Barb AW, Zhou P. 6.  2008. Mechanism and inhibition of LpxC: an essential zinc-dependent deacetylase of bacterial lipid A synthesis. Curr. Pharm. Biotechnol. 9:19–15 [Google Scholar]
  7. Bartling CM, Raetz CRH. 7.  2009. Crystal structure and acyl chain selectivity of Escherichia coli LpxD, the N-acyltransferase of lipid A biosynthesis. Biochemistry 48:368672–83 [Google Scholar]
  8. Bayer ME. 8.  1991. Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. J. Struct. Biol. 107:3268–80 [Google Scholar]
  9. Birck MR, Holler TP, Woodard RW. 9.  2000. Identification of a slow tight-binding inhibitor of 3-deoxy-d-manno-octulosonic acid 8-phosphate synthase. J. Am. Chem. Soc. 122:389334–35 [Google Scholar]
  10. Bishop RE. 10.  2008. Structural biology of membrane-intrinsic β-barrel enzymes: sentinels of the bacterial outer membrane. Biochim. Biophys. Acta Biomembr. 1778:91881–96 [Google Scholar]
  11. Bishop RE, Gibbons HS, Guina T, Trent MS, Miller SI, Raetz CR. 11.  2000. Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J. 19:195071–80 [Google Scholar]
  12. Bogdanov M, Xie J, Heacock P, Dowhan W. 12.  2008. To flip or not to flip: Lipid-protein charge interactions are a determinant of final membrane protein topology. J. Cell Biol. 182:5925–35 [Google Scholar]
  13. Bohin JP, Kennedy EP. 13.  1984. Regulation of the synthesis of membrane-derived oligosaccharides in Escherichia coli: assay of phosphoglycerol transferase I in vivo. J. Biol. Chem. 259:138388–93 [Google Scholar]
  14. Bos MP, Tefsen B, Geurtsen J, Tommassen J. 14.  2004. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. PNAS 101:259417–22 [Google Scholar]
  15. Braun M, Silhavy TJ. 15.  2002. Imp/OstA is required for cell envelope biogenesis in Escherichia coli. Mol. Microbiol. 45:51289–302 [Google Scholar]
  16. Braun V, Bosch V. 16.  1972. Sequence of the murein-lipoprotein and the attachment site of the lipid. Eur. J. Biochem. FEBS. 28:151–69 [Google Scholar]
  17. Brown MF, Reilly U, Abramite JA, Arcari JT, Oliver R. 17.  et al. 2012. Potent inhibitors of LpxC for the treatment of gram-negative infections. J. Med. Chem. 55:2914–23 [Google Scholar]
  18. Buetow L, Smith TK, Dawson A, Fyffe S, Hunter WN. 18.  2007. Structure and reactivity of LpxD, the N-acyltransferase of lipid A biosynthesis. PNAS 104:114321–26 [Google Scholar]
  19. Carpenter CD, Cooley BJ, Needham BD, Fisher CR, Trent MS. 19.  et al. 2014. The Vps/VacJ ABC transporter is required for intercellular spread of Shigella flexneri. Infect. Immun. 82:2660–69 [Google Scholar]
  20. Castuma CE, Crooke E, Kornberg A. 20.  1993. Fluid membranes with acidic domains activate DnaA, the initiator protein of replication in Escherichia coli. J. Biol. Chem. 268:3324665–68 [Google Scholar]
  21. Chng S-S, Gronenberg LS, Kahne D. 21.  2010. Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49:224565–67 [Google Scholar]
  22. Chong Z-S, Woo W-F, Chng S-S. 22.  2015. Osmoporin OmpC forms a complex with MlaA to maintain outer membrane lipid asymmetry in Escherichia coli. Mol. Microbiol. 98:61133–46 [Google Scholar]
  23. Chung HS, Raetz CR. 23.  2011. Dioxygenases in Burkholderia ambifaria and Yersinia pestis that hydroxylate the outer Kdo unit of lipopolysaccharide. PNAS 108:510–15 [Google Scholar]
  24. Cipolla L, Polissi A, Airoldi C, Galliani P, Sperandeo P, Nicotra F. 24.  2009. The Kdo biosynthetic pathway toward OM biogenesis as target in antibacterial drug design and development. Curr. Drug Discov. Technol. 6:119–33 [Google Scholar]
  25. Claesson A, Jansson AM, Pring BG, Hammond SM, Ekström B. 25.  1987. Design and synthesis of peptide derivatives of a 3-deoxy-d-manno-2-octulosonic acid (KDO) analogue as novel antibacterial agents acting upon lipopolysaccharide biosynthesis. J. Med. Chem. 30:122309–13 [Google Scholar]
  26. Claesson A, Luthman K, Gustafsson K, Bondesson G. 26.  1987. A 2-deoxy analogue of KDO as the first inhibitor of the enzyme CMP-KDO synthetase. Biochem. Biophys. Res. Commun. 143:31063–68 [Google Scholar]
  27. Coats SR, Berezow AB, To TT, Jain S, Bainbridge BW. 27.  et al. 2011. The lipid A phosphate position determines differential host toll-like receptor 4 responses to phylogenetically related symbiotic and pathogenic bacteria. Infect. Immun. 79:1203–10 [Google Scholar]
  28. Cowles CE, Li Y, Semmelhack MF, Cristea IM, Silhavy TJ. 28.  2011. The free and bound forms of Lpp occupy distinct subcellular locations in Escherichia coli. Mol. Microbiol. 79:51168–81 [Google Scholar]
  29. Cullen PA, Haake DA, Adler B. 29.  2004. Outer membrane proteins of pathogenic spirochetes. FEMS Microbiol. Rev. 28:3291–318 [Google Scholar]
  30. Cullen TW, Giles DK, Wolf LN, Ecobichon C, Boneca IG, Trent MS. 30.  2011. Helicobacter pylori versus the host: Remodeling of the bacterial outer membrane is required for survival in the gastric mucosa. PLOS Pathog 7:12e1002454 [Google Scholar]
  31. Cullen TW, Schofield WB, Barry NA, Putnam EE, Rundell EA. 31.  et al. 2015. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347:6218170–75 [Google Scholar]
  32. Dalebroux ZD, Edrozo MB, Pfuetzner RA, Ressl S, Kulasekara BR. 32.  et al. 2015. Delivery of cardiolipins to the Salmonella outer membrane is necessary for survival within host tissues and virulence. Cell Host Microbe 17:4441–51 [Google Scholar]
  33. Dalebroux ZD, Matamouros S, Whittington D, Bishop RE, Miller SI. 33.  2014. PhoPQ regulates acidic glycerophospholipid content of the Salmonella Typhimurium outer membrane. PNAS 111:51963–68 [Google Scholar]
  34. Darveau RP, Chilton PM. 34.  2013. Naturally occurring low biological reactivity lipopolysaccharides as vaccine adjuvants. Expert Rev. Vaccines 12:7707–9 [Google Scholar]
  35. De Vrije T, de Swart RL, Dowhan W, Tommassen J, de Kruijff B. 35.  1988. Phosphatidylglycerol is involved in protein translocation across Escherichia coli inner membranes. Nature 334:6178173–75 [Google Scholar]
  36. Dekker N. 36.  2000. Outer-membrane phospholipase A: known structure, unknown biological function. Mol. Microbiol. 35:4711–17 [Google Scholar]
  37. Doerrler WT, Gibbons HS, Raetz CRH. 37.  2004. MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J. Biol. Chem. 279:4345102–9 [Google Scholar]
  38. Doerrler WT, Reedy MC, Raetz CR. 38.  2001. An Escherichia coli mutant defective in lipid export. J. Biol. Chem. 276:1511461–64 [Google Scholar]
  39. Dong H, Xiang Q, Gu Y, Wang Z, Paterson NG. 39.  et al. 2014. Structural basis for outer membrane lipopolysaccharide insertion. Nature 511:750752–56 [Google Scholar]
  40. Donohue-Rolfe AM, Schaechter M. 40.  1980. Translocation of phospholipids from the inner to the outer membrane of Escherichia coli. PNAS 77:41867–71 [Google Scholar]
  41. Dowhan W. 41.  2014. Lipids and extracellular materials. Annu. Rev. Biochem. 83:145–49 [Google Scholar]
  42. Dowhan W, Bogdanov M. 42.  2009. Lipid-dependent membrane protein topogenesis. Annu. Rev. Biochem. 78:515–40 [Google Scholar]
  43. Eckford PDW, Sharom FJ. 43.  2008. Functional characterization of Escherichia coli MsbA: interaction with nucleotides and substrates. J. Biol. Chem. 283:1912840–50 [Google Scholar]
  44. Ernst RK, Yi EC, Guo L, Lim KB, Burns JL. 44.  et al. 1999. Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286:54441561–65 [Google Scholar]
  45. Ferrari G, Garaguso I, Adu-Bobie J, Doro F, Taddei AR. 45.  et al. 2006. Outer membrane vesicles from group B Neisseria meningitidis Δgna33 mutant: proteomic and immunological comparison with detergent-derived outer membrane vesicles.. PROTEOMICS 6:61856–66 [Google Scholar]
  46. Francisco JA, Earhart CF, Georgiou G. 46.  1992. Transport and anchoring of beta-lactamase to the external surface of Escherichia coli. PNAS 89:72713–17 [Google Scholar]
  47. Frasch CE. 47.  2009. Preparation of bacterial polysaccharide-protein conjugates: analytical and manufacturing challenges. Vaccine 27:466468–70 [Google Scholar]
  48. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R. 48.  et al. 1997. Genomic sequence of a lyme disease spirochaete, Borrelia burgdorferi. Nature 390:6660580–86 [Google Scholar]
  49. Fraser CM, Norris SJ, Weinstock GM, White O, Sutton GG. 49.  et al. 1998. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281:5375375–88 [Google Scholar]
  50. Freinkman E, Chng S-S, Kahne D. 50.  2011. The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. PNAS 108:62486–91 [Google Scholar]
  51. Freinkman E, Okuda S, Ruiz N, Kahne D. 51.  2012. Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry 51:244800–6 [Google Scholar]
  52. Galen JE, Zhao L, Chinchilla M, Wang JY, Pasetti MF. 52.  et al. 2004. Adaptation of the endogenous Salmonella enterica serovar Typhi clyA-encoded hemolysin for antigen export enhances the immunogenicity of anthrax protective antigen domain 4 expressed by the attenuated live-vector vaccine strain CVD 908-htrA. Infect. Immun. 72:127096–106 [Google Scholar]
  53. Garçon N. 53.  2010. Preclinical development of AS04. Vaccine Adjuvants: Methods and Protocols G Davies 15–27 New York: Humana [Google Scholar]
  54. Garner J, Crooke E. 54.  1996. Membrane regulation of the chromosomal replication activity of E. coli DnaA requires a discrete site on the protein. EMBO J. 15:92313–21 [Google Scholar]
  55. Gorringe AR, Pajón R. 55.  2012. Bexsero. Hum. Vaccines Immunother. 8:2174–83 [Google Scholar]
  56. Grabowicz M, Yeh J, Silhavy TJ. 56.  2013. Dominant negative lptE mutation that supports a role for LptE as a plug in the LptD barrel. J. Bacteriol. 195:61327–34 [Google Scholar]
  57. Gronenberg LS, Kahne D. 57.  2010. Development of an activity assay for discovery of inhibitors of lipopolysaccharide transport. J. Am. Chem. Soc. 132:82518–19 [Google Scholar]
  58. Gruss F, Zähringer F, Jakob RP, Burmann BM, Hiller S, Maier T. 58.  2013. The structural basis of autotransporter translocation by TamA. Nat. Struct. Mol. Biol. 20:111318–20 [Google Scholar]
  59. Hantke K, Braun V. 59.  1973. Covalent binding of lipid to protein. Eur. J. Biochem. 34:2284–96 [Google Scholar]
  60. Hittle LE, Powell DA, Jones JW, Tofigh M, Goodlett DR. 60.  et al. 2015. Site-specific activity of the acyltransferases HtrB1 and HtrB2 in Pseudomonas aeruginosa lipid A biosynthesis. Pathog. Dis. 73:8ftv053 [Google Scholar]
  61. Holst J, Martin D, Arnold R, Huergo CC, Oster P. 61.  et al. 2009. Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis. Vaccine 27:Supp. 2B3–12 [Google Scholar]
  62. Ismaili J, Rennesson J, Aksoy E, Vekemans J, Vincart B. 62.  et al. 2002. Monophosphoryl lipid A activates both human dendritic cells and T cells. J. Immunol. 168:2926–32 [Google Scholar]
  63. Jackson BJ, Bohin JP, Kennedy EP. 63.  1984. Biosynthesis of membrane-derived oligosaccharides: characterization of mdoB mutants defective in phosphoglycerol transferase I activity. J. Bacteriol. 160:3976–81 [Google Scholar]
  64. Jackson BJ, Kennedy EP. 64.  1983. The biosynthesis of membrane-derived oligosaccharides: a membrane-bound phosphoglycerol transferase. J. Biol. Chem. 258:42394–98 [Google Scholar]
  65. Jenkins RJ, Dotson GD. 65.  2012. Dual targeting antibacterial peptide inhibitor of early lipid A biosynthesis. ACS Chem. Biol. 7:71170–77 [Google Scholar]
  66. Kamio Y, Nikaido H. 66.  1976. Outer membrane of Salmonella typhimurium: Accessibility of phospholipid head groups to phospholipase C and cyanogen bromide activated dextran in the external medium. Biochemistry 15:122561–70 [Google Scholar]
  67. Kanfer J, Kennedy EP. 67.  1964. Metabolism and function of bacterial lipids: II. Biosynthesis of phospholipids in Escherichia coli. J. Biol. Chem. 239:1720–26 [Google Scholar]
  68. Kawahara K, Seydel U, Matsuura M, Danbara H, Rietschel ET, Zähringer U. 68.  1991. Chemical structure of glycosphingolipids isolated from Sphingomonas paucimobilis. FEBS Lett. 292:1–2107–10 [Google Scholar]
  69. Kawasaki S, Moriguchi R, Sekiya K, Nakai T, Ono E. 69.  et al. 1994. The cell envelope structure of the lipopolysaccharide-lacking gram-negative bacterium Sphingomonas paucimobilis. J. Bacteriol. 176:2284–90 [Google Scholar]
  70. Kellenberger E. 70.  1990. The “Bayer bridges” confronted with results from improved electron microscopy methods. Mol. Microbiol. 4:5697–705 [Google Scholar]
  71. Kesty NC, Kuehn MJ. 71.  2004. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 279:32069–76 [Google Scholar]
  72. Kim JH, Lee J, Park J, Gho YS. 72.  2015. Gram-negative and gram-positive bacterial extracellular vesicles. Semin. Cell Dev. Biol. 40:97–104 [Google Scholar]
  73. Kulkarni HM, Jagannadham MV. 73.  2014. Biogenesis and multifaceted roles of outer membrane vesicles from gram-negative bacteria. Microbiology 160:Part 102109–21 [Google Scholar]
  74. Lee C-J, Liang X, Chen X, Zeng D, Joo SH. 74.  et al. 2011. Species-specific and inhibitor-dependent conformations of LpxC: implications for antibiotic design. Chem. Biol. 18:138–47 [Google Scholar]
  75. Lee C-J, Liang X, Gopalaswamy R, Najeeb J, Ark ED. 75.  et al. 2014. Structural basis of the promiscuous inhibitor susceptibility of Escherichia coli LpxC. ACS Chem. Biol. 9:1237–46 [Google Scholar]
  76. Lee C-J, Liang X, Wu Q, Najeeb J, Zhao J. 76.  et al. 2016. Drug design from the cryptic inhibitor envelope. Nat. Commun. 7:10638 [Google Scholar]
  77. Liang X, Lee C-J, Chen X, Chung HS, Zeng D. 77.  et al. 2011. Syntheses, structures and antibiotic activities of LpxC inhibitors based on the diacetylene scaffold. Bioorg. Med. Chem. 19:2852–60 [Google Scholar]
  78. Liang X, Lee C-J, Zhao J, Toone EJ, Zhou P. 78.  2013. Synthesis, structure, and antibiotic activity of aryl-substituted LpxC inhibitors. J. Med. Chem. 56:176954–66 [Google Scholar]
  79. Lill R, Dowhan W, Wickner W. 79.  1990. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60:2271–80 [Google Scholar]
  80. Lu Y-H, Guan Z, Zhao J, Raetz CRH. 80.  2011. Three phosphatidylglycerol-phosphate phosphatases in the inner membrane of Escherichia coli. J. Biol. Chem. 286:75506–18 [Google Scholar]
  81. Malinverni JC, Silhavy TJ. 81.  2009. An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. PNAS 106:198009–14 [Google Scholar]
  82. Mansoor UF, Vitharana D, Reddy PA, Daubaras DL, McNicholas P. 82.  et al. 2011. Design and synthesis of potent gram-negative specific LpxC inhibitors. Bioorg. Med. Chem. Lett. 21:41155–61 [Google Scholar]
  83. Mata-Haro V, Cekic C, Martin M, Chilton PM, Casella CR, Mitchell TC. 83.  2007. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316:58311628–32 [Google Scholar]
  84. Matsumoto K. 84.  2001. Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol. Microbiol. 39:61427–33 [Google Scholar]
  85. McClerren AL, Endsley S, Bowman JL, Andersen NH, Guan Z. 85.  et al. 2005. A slow, tight-binding inhibitor of the zinc-dependent deacetylase LpxC of lipid A biosynthesis with antibiotic activity comparable to ciprofloxacin. Biochemistry 44:5016574–83 [Google Scholar]
  86. Miller KJ, Kennedy EP. 86.  1987. Transfer of phosphoethanolamine residues from phosphatidylethano-lamine to the membrane-derived oligosaccharides of Escherichia coli. J. Bacteriol. 169:2682–86 [Google Scholar]
  87. Moffatt JH, Harper M, Harrison P, Hale JDF, Vinogradov E. 87.  et al. 2010. Colistin resistance in Acinetobacter baumannii is mediated by complete loss of lipopolysaccharide production. Antimicrob. Agents Chemother. 54:124971–77 [Google Scholar]
  88. Nakayama H, Kurokawa K, Lee BL. 88.  2012. Lipoproteins in bacteria: Structures and biosynthetic pathways. FEBS J. 279:234247–68 [Google Scholar]
  89. Narita S, Tokuda H. 89.  2009. Biochemical characterization of an abc transporter lptbfgc complex required for the outer membrane sorting of lipopolysaccharides. FEBS Lett. 583:132160–64 [Google Scholar]
  90. Nayar AS, Dougherty TJ, Ferguson KE, Granger BA, McWilliams L. 90.  et al. 2015. Novel antibacterial targets and compounds revealed by a high-throughput cell wall reporter assay. J. Bacteriol. 197:101726–34 [Google Scholar]
  91. Needham BD, Carroll SM, Giles DK, Georgiou G, Whiteley M, Trent MS. 91.  2013. Modulating the innate immune response by combinatorial engineering of endotoxin. PNAS 110:41464–69 [Google Scholar]
  92. Needham BD, Trent MS. 92.  2013. Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat. Rev. Microbiol. 11:7467–81 [Google Scholar]
  93. Nguyen BD, Cunningham D, Liang X, Chen X, Toone EJ. 93.  et al. 2011. Lipooligosaccharide is required for the generation of infectious elementary bodies in Chlamydia trachomatis. PNAS 108:2510284–89 [Google Scholar]
  94. Noinaj N, Kuszak AJ, Gumbart JC, Lukacik P, Chang H. 94.  et al. 2013. Structural insight into the biogenesis of β-barrel membrane proteins. Nature 501:7467385–90 [Google Scholar]
  95. Okemoto K, Kawasaki K, Hanada K, Miura M, Nishijima M. 95.  2006. A potent adjuvant monophosphoryl lipid A triggers various immune responses, but not secretion of IL-1β or activation of caspase-1. J. Immunol. 176:21203–8 [Google Scholar]
  96. Okuda S, Freinkman E, Kahne D. 96.  2012. Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338:61111214–17 [Google Scholar]
  97. Osman C, Haag M, Wieland FT, Brügger B, Langer T. 97.  2010. A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J. 29:121976–87 [Google Scholar]
  98. Peng D, Hong W, Choudhury BP, Carlson RW, Gu X-X. 98.  2005. Moraxella catarrhalis bacterium without endotoxin, a potential vaccine candidate. Infect. Immun. 73:117569–77 [Google Scholar]
  99. Phillips NJ, Adin DM, Stabb EV, McFall-Ngai MJ, Apicella MA, Gibson BW. 99.  2011. The lipid A from Vibrio fischeri lipopolysaccharide: a unique structure bearing a phosphoglycerol moiety. J. Biol. Chem. 286:2421203–19 [Google Scholar]
  100. Pride AC, Guan Z, Trent MS. 100.  2014. Characterization of the Vibrio cholerae VolA surface-exposed lipoprotein lysophospholipase. J. Bacteriol. 196:81619–26 [Google Scholar]
  101. Pring BG, Jansson AM, Persson K, Andersson I, Gagner-Milchert I. 101.  et al. 1989. Synthesis of 8-substituted derivatives of the 2-deoxy analogue of 3-deoxy-β-d-manno-2-octulopyranosonic acid (2-deoxy-beta-KDO) as inhibitors of 3-deoxy-d-manno-octulosonate cytidylyltransferase. J. Med. Chem. 32:51069–74 [Google Scholar]
  102. Qureshi N, Takayama K, Ribi E. 102.  1982. Purification and structural determination of nontoxic lipid A obtained from the lipopolysaccharide of Salmonella typhimurium. J. Biol. Chem. 257:1911808–15 [Google Scholar]
  103. Raetz CR. 103.  1986. Molecular genetics of membrane phospholipid synthesis. Annu. Rev. Genet. 20:253–95 [Google Scholar]
  104. Raetz CR, Roderick SL. 104.  1995. A left-handed parallel β helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science 270:5238997–1000 [Google Scholar]
  105. Raetz CRH, Reynolds CM, Trent MS, Bishop RE. 105.  2007. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76:1295–329 [Google Scholar]
  106. Raetz CRH, Whitfield C. 106.  2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635–700 [Google Scholar]
  107. Reyes CL, Chang G. 107.  2005. Structure of the ABC transporter MsbA in complex with ADP·vanadate and lipopolysaccharide. Science 308:57241028–31 [Google Scholar]
  108. Roier S, Blume T, Klug L, Wagner GE, Elhenawy W. 108.  et al. 2015. A basis for vaccine development: comparative characterization of Haemophilus influenzae outer membrane vesicles. Int. J. Med. Microbiol. 305:3298–309 [Google Scholar]
  109. Rubin EJ, O'Brien JP, Ivanov PL, Brodbelt JS, Trent MS. 109.  2014. Identification of a broad family of lipid A late acyltransferases with non-canonical substrate specificity. Mol. Microbiol. 91:5887–99 [Google Scholar]
  110. Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ. 110.  2008. Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. PNAS 105:145537–42 [Google Scholar]
  111. Salkowski CA, Detore GR, Vogel SN. 111.  1997. Lipopolysaccharide and monophosphoryl lipid A differentially regulate interleukin-12, gamma interferon, and interleukin-10 mRNA production in murine macrophages. Infect. Immun. 65:83239–47 [Google Scholar]
  112. Schroeder J, Aebischer T. 112.  2009. Recombinant outer membrane vesicles to augment antigen-specific live vaccine responses. Vaccine 27:486748–54 [Google Scholar]
  113. Schwechheimer C, Kuehn MJ. 113.  2015. Outer-membrane vesicles from gram-negative bacteria: biogenesis and functions. Nat. Rev. Microbiol. 13:10605–19 [Google Scholar]
  114. Sherman DJ, Okuda S, Denny WA, Kahne D. 114.  2013. Validation of inhibitors of an ABC transporter required to transport lipopolysaccharide to the cell surface in Escherichia coli. Bioorg. Med. Chem. 21:164846–51 [Google Scholar]
  115. Silipo A, Vitiello G, Gully D, Sturiale L, Chaintreuil C. 115.  et al. 2014. Covalently linked hopanoid-lipid A improves outer-membrane resistance of a Bradyrhizobium symbiont of legumes. Nat. Commun. 5:5106 [Google Scholar]
  116. Smith WP, Tai PC, Davis BD. 116.  1981. Bacillus licheniformis penicillinase: cleavages and attachment of lipid during cotranslational secretion. PNAS 78:63501–5 [Google Scholar]
  117. Snijder HJ, Dijkstra BW. 117.  2000. Bacterial phospholipase A: Structure and function of an integral membrane phospholipase. Biochim. Biophys. Acta 1488:1–291–101 [Google Scholar]
  118. Sohlenkamp C, Geiger O. 118.  2016. Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol. Rev. 40:1133–59 [Google Scholar]
  119. Sperandeo P, Cescutti R, Villa R, Benedetto CD, Candia D. 119.  et al. 2007. Characterization of LptA and LptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J. Bacteriol. 189:1244–53 [Google Scholar]
  120. Sperandeo P, Lau FK, Carpentieri A, Castro CD, Molinaro A. 120.  et al. 2008. Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J. Bacteriol. 190:134460–69 [Google Scholar]
  121. Sperandeo P, Pozzi C, Dehò G, Polissi A. 121.  2006. Non-essential KDO biosynthesis and new essential cell envelope biogenesis genes in the Escherichia coli yrbG-yhbG locus. Res. Microbiol. 157:6547–58 [Google Scholar]
  122. Srinivas N, Jetter P, Ueberbacher BJ, Werneburg M, Zerbe K. 122.  et al. 2010. Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science 327:59681010–13 [Google Scholar]
  123. Steeghs L, den Hartog R, den Boer A, Zomer B, Roholl P, van der Ley P. 123.  1998. Meningitis bacterium is viable without endotoxin. Nature 392:6675449–50 [Google Scholar]
  124. Sutterlin HA, Shi H, May KL, Miguel A, Khare S. 124.  et al. 2016. Disruption of lipid homeostasis in the gram-negative cell envelope activates a novel cell death pathway. PNAS 113:E1565–74 [Google Scholar]
  125. Tamura Y, Harada Y, Nishikawa S, Yamano K, Kamiya M. 125.  et al. 2013. Tam41 is a CDP-diacylglycerol synthase required for cardiolipin biosynthesis in mitochondria. Cell Metab. 17:5709–18 [Google Scholar]
  126. Tan BK, Bogdanov M, Zhao J, Dowhan W, Raetz CRH, Guan Z. 126.  2012. Discovery of a cardiolipin synthase utilizing phosphatidylethanolamine and phosphatidylglycerol as substrates. PNAS 109:4116504–9 [Google Scholar]
  127. Tani C, Stella M, Donnarumma D, Biagini M, Parente P. 127.  et al. 2014. Quantification by LC–MSE of outer membrane vesicle proteins of the Bexsero® vaccine. Vaccine 32:111273–79 [Google Scholar]
  128. Tefsen B, Bos MP, Beckers F, Tommassen J, de Cock H. 128.  2005. MsbA is not required for phospholipid transport in Neisseria meningitidis. J. Biol. Chem. 280:4335961–66 [Google Scholar]
  129. Thompson BS, Chilton PM, Ward JR, Evans JT, Mitchell TC. 129.  2005. The low-toxicity versions of LPS, MPL® adjuvant and RC529, are efficient adjuvants for CD4+ T cells. J. Leukoc. Biol. 78:61273–80 [Google Scholar]
  130. Tokunaga M, Tokunaga H, Wu HC. 130.  1982. Post-translational modification and processing of Escherichia coli prolipoprotein in vitro. PNAS 79:72255–59 [Google Scholar]
  131. Tomaras AP, McPherson CJ, Kuhn M, Carifa A, Mullins L. 131.  et al. 2014. LpxC inhibitors as new antibacterial agents and tools for studying regulation of lipid A biosynthesis in gram-negative pathogens. mBio 5:5e01551–14 [Google Scholar]
  132. Tran AX, Dong C, Whitfield C. 132.  2010. Structure and functional analysis of LptC, a conserved membrane protein involved in the lipopolysaccharide export pathway in Escherichia coli. J. Biol. Chem. 285:4333529–39 [Google Scholar]
  133. Trent MS, Stead CM, Tran AX, Hankins JV. 133.  2006. Diversity of endotoxin and its impact on pathogenesis. J. Endotoxin Res. 12:4205–23 [Google Scholar]
  134. Urfer M, Bogdanovic J, Lo Monte F, Moehle K, Zerbe K. 134.  et al. 2016. A peptidomimetic antibiotic targets outer membrane proteins and disrupts selectively the outer membrane in Escherichia coli. J. Biol. Chem. 291:41921–32 [Google Scholar]
  135. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. 135.  2008. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. PNAS 105:5220858–63 [Google Scholar]
  136. Vamadevan AS, Fukata M, Arnold ET, Thomas LS, Hsu D, Abreu MT. 136.  2010. Regulation of TLR4-associated MD-2 in intestinal epithelial cells: a comprehensive analysis. Innate Immun. 16:293–103 [Google Scholar]
  137. van de Waterbeemd B, Streefland M, van der Ley P, Zomer B, van Dijken H. 137.  et al. 2010. Improved OMV vaccine against Neisseria meningitidis using genetically engineered strains and a detergent-free purification process. Vaccine 28:304810–16 [Google Scholar]
  138. van der Ley P, van den Dobbelsteen G. 138.  2011. Next-generation outer membrane vesicle vaccines against Neisseria meningitidis based on nontoxic LPS mutants. Hum. Vaccin. 7:8886–90 [Google Scholar]
  139. Vorachek-Warren MK, Ramirez S, Cotter RJ, Raetz CRH. 139.  2002. A triple mutant of Escherichia coli lacking secondary acyl chains on lipid A. J. Biol. Chem. 277:1614194–205 [Google Scholar]
  140. Vozza N, Feldman M. 140.  2015. Glyco-engineering O-antigen-based vaccines and diagnostics in E. coli. Glyco-Engineering A Castilho 57–70 New York: Springer [Google Scholar]
  141. Wai SN, Lindmark B, Söderblom T, Takade A, Westermark M. 141.  et al. 2003. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:125–35 [Google Scholar]
  142. Wang X, Bogdanov M, Dowhan W. 142.  2002. Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. EMBO J. 21:215673–81 [Google Scholar]
  143. Werneburg M, Zerbe K, Juhas M, Bigler L, Stalder U. 143.  et al. 2012. Inhibition of lipopolysaccharide transport to the outer membrane in Pseudomonas aeruginosa by peptidomimetic antibiotics. Chembiochem Eur. J. Chem. Biol. 13:121767–75 [Google Scholar]
  144. White KA, Lin S, Cotter RJ, Raetz CR. 144.  1999. A Haemophilus influenzae gene that encodes a membrane bound 3-deoxy-d-manno-octulosonic acid (Kdo) kinase: possible involvement of Kdo phosphorylation in bacterial virulence. J. Biol. Chem. 274:4431391–400 [Google Scholar]
  145. Whitfield C, Trent MS. 145.  2014. Biosynthesis and export of bacterial lipopolysaccharides. Annu. Rev. Biochem. 83:199–128 [Google Scholar]
  146. Woebking B, Reuter G, Shilling RA, Velamakanni S, Shahi S. 146.  et al. 2005. Drug-lipid A interactions on the Escherichia coli ABC transporter Msb. J. Bacteriol. 187:186363–69 [Google Scholar]
  147. Wu HC, Lai JS, Hayashi S, Giam CZ. 147.  1982. Biogenesis of membrane lipoproteins in Escherichia coli. Biophys. J. 37:1307–15 [Google Scholar]
  148. Xia W, Dowhan W. 148.  1995. In vivo evidence for the involvement of anionic phospholipids in initiation of DNA replication in Escherichia coli. PNAS 92:3783–87 [Google Scholar]
  149. Xu X, Wang J, Grison C, Petek S, Coutrot P. 149.  et al. 2003. Structure-based design of novel inhibitors of 3-deoxy-d-manno-octulosonate 8-phosphate synthase. Drug Des. Discov. 18:2–391–99 [Google Scholar]
  150. Yakushi T, Masuda K, Narita S, Matsuyama S, Tokuda H. 150.  2000. A new ABC transporter mediating the detachment of lipid-modified proteins from membranes. Nat. Cell Biol. 2:4212–18 [Google Scholar]
  151. Young HE, Zhao J, Barker JR, Guan Z, Valdivia RH, Zhou P. 151.  2016. Discovery of the elusive UDP-diacylglucosamine hydrolase in the lipid A biosynthetic pathway in Chlamydia trachomatis. mBio 7:e00090–16 [Google Scholar]
  152. Zhang J, Guan Z, Murphy AN, Wiley SE, Perkins GA. 152.  et al. 2011. Mitochondrial phosphatase PTPMT1 is essential for cardiolipin biosynthesis. Cell Metab. 13:6690–700 [Google Scholar]
  153. Zhang W, Campbell HA, King SC, Dowhan W. 153.  2005. Phospholipids as determinants of membrane protein topology: Phosphatidylethanolamine is required for the proper topological organization of the gamma-aminobutyric acid permease (GabP) of Escherichia coli. J. Biol. Chem. 280:2826032–38 [Google Scholar]
/content/journals/10.1146/annurev-micro-102215-095308
Loading
The Power of Asymmetry: Architecture and Assembly of the Gram-Negative Outer Membrane Lipid Bilayer
Annual Review of Microbiology 70, 255 (2016); https://doi.org/10.1146/annurev-micro-102215-095308
/content/journals/10.1146/annurev-micro-102215-095308
/content/journals/10.1146/annurev-micro-102215-095308
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error