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Annual Review of Biochemistry

Volume 76, 2007

Lipid A Modification Systems in Gram-Negative Bacteria

Abstract

Abstract

The lipid A moiety of lipopolysaccharide forms the outer monolayer of the outer membrane of most gram-negative bacteria. lipid A is synthesized on the cytoplasmic surface of the inner membrane by a conserved pathway of nine constitutive enzymes. Following attachment of the core oligosaccharide, nascent core-lipid A is flipped to the outer surface of the inner membrane by the ABC transporter MsbA, where the O-antigen polymer is attached. Diverse covalent modifications of the lipid A moiety may occur during its transit from the outer surface of the inner membrane to the outer membrane. Lipid A modification enzymes are reporters for lipopolysaccharide trafficking within the bacterial envelope. Modification systems are variable and often regulated by environmental conditions. Although not required for growth, the modification enzymes modulate virulence of some gram-negative pathogens. Heterologous expression of lipid A modification enzymes may enable the development of new vaccines.

Keyword(s): endotoxin, innate immunity, lipopolysaccharide, LpxC, MsbA
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2007-07-07
2024-06-15
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Literature Cited

  1. Fahy E, Subramaniam S, Brown HA, Glass CK, Merrill AHJ. et al. 2005. J. Lipid Res. 46:839–62 [Google Scholar]
  2. Raetz CRH, Whitfield C. 2002. Annu. Rev. Biochem. 71:635–700 [Google Scholar]
  3. Brade H, Opal SM, Vogel SN, Morrison DC. eds. 1999. Endotoxin in Health and Disease New York: Marcel Dekker.950 pp [Google Scholar]
  4. Nikaido H. 2003. Microbiol. Mol. Biol. Rev. 67:593–656 [Google Scholar]
  5. Galloway SM, Raetz CRH. 1990. J. Biol. Chem. 265:6394–402 [Google Scholar]
  6. Guan Z, Breazeale SD, Raetz CRH. 2005. Anal. Biochem. 345:336–39 [Google Scholar]
  7. Steeghs L, de Cock H, Evers E, Zomer B, Tommassen J, van der Ley P. 2001. EMBO J. 20:6937–45 [Google Scholar]
  8. Meredith TC, Aggarwal P, Mamat U, Lindner B, Woodard RW. 2006. ACS Chem. Biol. 1:33–42 [Google Scholar]
  9. Belunis CJ, Clementz T, Carty SM, Raetz CRH. 1995. J. Biol. Chem. 270:27646–52 [Google Scholar]
  10. Onishi HR, Pelak BA, Gerckens LS, Silver LL, Kahan FM. et al. 1996. Science 274:980–82 [Google Scholar]
  11. Bos MP, Robert V, Tommassen J. 2007. Annu. Rev. Microbiol. 61: In press [Google Scholar]
  12. Poltorak A, He X, Smirnova I, Liu MY, Huffel CV. et al. 1998. Science 282:2085–88 [Google Scholar]
  13. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T. et al. 1999. J. Immunol. 162:3749–52 [Google Scholar]
  14. Shimazu R, Akashi S, Ogata H, Nagai Y, Fukudome K. et al. 1999. J. Exp. Med. 189:1777–82 [Google Scholar]
  15. Gangloff M, Gay NJ. 2004. Trends Biochem. Sci. 29:294–300 [Google Scholar]
  16. Miller SI, Ernst RK, Bader MW. 2005. Nat. Rev. Microbiol. 3:36–46 [Google Scholar]
  17. Visintin A, Halmen KA, Latz E, Monks BG, Golenbock DT. 2005. J. Immunol. 175:6465–72 [Google Scholar]
  18. Akira S, Uematsu S, Takeuchi O. 2006. Cell 124:783–801 [Google Scholar]
  19. Beutler B, Cerami A. 1988. Annu. Rev. Biochem. 57:505–18 [Google Scholar]
  20. Dinarello CA. 1991. Blood 77:1627–52 [Google Scholar]
  21. Medzhitov R, Janeway CJ. 2000. N. Engl. J. Med. 343:338–44 [Google Scholar]
  22. van Duin D, Medzhitov R, Shaw AC. 2006. Trends Immunol. 27:49–55 [Google Scholar]
  23. Li A, Chang AC, Peer GT, Hinshaw LB, Taylor FBJ. 1996. Shock 5:274–79 [Google Scholar]
  24. Drake TA, Cheng J, Chang A, Taylor FBJ. 1993. Am. J. Pathol. 142:1458–70 [Google Scholar]
  25. Parillo JE. 1993. N. Engl. J. Med. 328:1471–77 [Google Scholar]
  26. Russell JA. 2006. N. Engl. J. Med. 355:1699–713 [Google Scholar]
  27. Rietschel ET, Kirikae T, Schade FU, Mamat U, Schmidt G. et al. 1994. FASEB J. 8:217–25 [Google Scholar]
  28. Prabhakar U, Conway TM, Murdock P, Mooney JL, Clark S. et al. 2005. DNA Cell Biol. 24:410–31 [Google Scholar]
  29. Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV. et al. 2005. Nature 437:1032–37 [Google Scholar]
  30. Qureshi N, Takayama K, Ribi E. 1982. J. Biol. Chem. 257:11808–15 [Google Scholar]
  31. Persing DH, Coler RN, Lacy MJ, Johnson DA, Baldridge JR. et al. 2002. Trends Microbiol. 10:S32–37 [Google Scholar]
  32. Baldridge JR, McGowan P, Evans JT, Cluff C, Mossman S. et al. 2004. Expert. Opin. Biol. Ther. 4:1129–38 [Google Scholar]
  33. Takayama K, Qureshi N, Beutler B, Kirkland TN. 1989. Infect. Immun. 57:1336–38 [Google Scholar]
  34. Golenbock DT, Hampton RY, Qureshi N, Takayama K, Raetz CRH. 1991. J. Biol. Chem. 266:19490–98 [Google Scholar]
  35. Christ WJ, Asano O, Robidoux AL, Perez M, Wang Y. et al. 1995. Science 265:80–83 [Google Scholar]
  36. Hawkins LD, Christ WJ, Rossignol DP. 2004. Curr. Top. Med. Chem. 4:1147–71 [Google Scholar]
  37. Lynn M, Rossignol DP, Wheeler JL, Kao RJ, Perdomo CA. et al. 2003. J. Infect. Dis. 187:631–39 [Google Scholar]
  38. Bell JK, Botos I, Hall PR, Askins J, Shiloach J. et al. 2005. Proc. Natl. Acad. Sci. USA 102:10976–80 [Google Scholar]
  39. Choe J, Kelker MS, Wilson IA. 2005. Science 309:581–85 [Google Scholar]
  40. Bell JK, Askins J, Hall PR, Davies DR, Segal DM. 2006. Proc. Natl. Acad. Sci. USA 103:8792–97 [Google Scholar]
  41. Raetz CRH. 1990. Annu. Rev. Biochem. 59:129–70 [Google Scholar]
  42. Gunn JS, Lim KB, Krueger J, Kim K, Guo L. et al. 1998. Mol. Microbiol. 27:1171–82 [Google Scholar]
  43. Guo L, Lim KB, Gunn JS, Bainbridge B, Darveau RP. et al. 1997. Science 276:250–53 [Google Scholar]
  44. Groisman EA. 2001. J. Bacteriol. 183:1835–42 [Google Scholar]
  45. Gibbons HS, Kalb SR, Cotter RJ, Raetz CRH. 2005. Mol. Microbiol. 55:425–40 [Google Scholar]
  46. Bader MW, Sanowar S, Daley ME, Schneider AR, Cho U. et al. 2005. Cell 122:461–72 [Google Scholar]
  47. Bishop RE, Gibbons HS, Guina T, Trent MS, Miller SI, Raetz CRH. 2000. EMBO J. 19:5071–80 [Google Scholar]
  48. Trent MS, Ribeiro AA, Lin S, Cotter RJ, Raetz CRH. 2001. J. Biol. Chem. 276:43122–31 [Google Scholar]
  49. Trent MS, Ribeiro AA, Doerrler WT, Lin S, Cotter RJ, Raetz CRH. 2001. J. Biol. Chem. 276:43132–44 [Google Scholar]
  50. Trent MS, Pabich W, Raetz CRH, Miller SI. 2001. J. Biol. Chem. 276:9083–92 [Google Scholar]
  51. Trent MS, Raetz CRH. 2002. J. Endotoxin Res. 8:158 [Google Scholar]
  52. Tran AX, Karbarz MJ, Wang X, Raetz CRH, McGrath SC. et al. 2004. J. Biol. Chem. 279:55780–91 [Google Scholar]
  53. Lee H, Hsu FF, Turk J, Groisman EA. 2004. J. Bacteriol. 186:4124–33 [Google Scholar]
  54. Reynolds CM, Kalb SR, Cotter RJ, Raetz CRH. 2005. J. Biol. Chem. 280:21202–11 [Google Scholar]
  55. Reynolds CM, Ribeiro AA, McGrath SC, Cotter RJ, Raetz CRH, Trent MS. 2006. J. Biol. Chem. 281:21974–87 [Google Scholar]
  56. Doerrler WT, Gibbons HS, Raetz CRH. 2004. J. Biol. Chem. 279:45102–9 [Google Scholar]
  57. Bos MP, Tefsen B, Geurtsen J, Tommassen J. 2004. Proc. Natl. Acad. Sci. USA 101:9417–22 [Google Scholar]
  58. Jia W, Zoeiby AE, Petruzziello TN, Jayabalasingham B, Seyedirashti S, Bishop RE. 2004. J. Biol. Chem. 279:44966–75 [Google Scholar]
  59. Wang X, Karbarz MJ, McGrath SC, Cotter RJ, Raetz CRH. 2004. J. Biol. Chem. 279:49470–78 [Google Scholar]
  60. Wang X, McGrath SC, Cotter RJ, Raetz CRH. 2006. J. Biol. Chem. 281:9321–30 [Google Scholar]
  61. Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, Kahne D. 2006. Proc. Natl. Acad. Sci. USA 103:11754–59 [Google Scholar]
  62. Nishijima M, Raetz CRH. 1979. J. Biol. Chem. 254:7837–44 [Google Scholar]
  63. Takayama K, Qureshi N, Mascagni P, Nashed MA, Anderson L, Raetz CRH. 1983. J. Biol. Chem. 258:7379–85 [Google Scholar]
  64. Bulawa CE, Raetz CRH. 1984. J. Biol. Chem. 259:4846–51 [Google Scholar]
  65. Imoto M, Kusumoto S, Shiba T, Naoki H, Iwashita T. et al. 1983. Tetrahedron Lett. 24:4017–20 [Google Scholar]
  66. Strain SM, Fesik SW, Armitage IM. 1983. J. Biol. Chem. 258:13466–77 [Google Scholar]
  67. Galanos C, Lüderitz O, Rietschel ET, Westphal O, Brade H. et al. 1985. Eur. J. Biochem. 148:1–5 [Google Scholar]
  68. Anderson MS, Bulawa CE, Raetz CRH. 1985. J. Biol. Chem. 260:15536–41 [Google Scholar]
  69. Ray BL, Painter G, Raetz CRH. 1984. J. Biol. Chem. 259:4852–59 [Google Scholar]
  70. Riley M, Abe T, Arnaud MB, Berlyn MK, Blattner FR. et al. 2006. Nucleic Acids Res. 34:1–9 [Google Scholar]
  71. Krziwon C, Zähringer U, Kawahara K, Weidemann B, Kusumoto S. et al. 1995. Infect. Immun. 63:2899–905 [Google Scholar]
  72. Wheeler DL, Church DM, Federhen S, Lash AE, Madden TL. et al. 2003. Nucleic Acids Res. 31:28–33 [Google Scholar]
  73. Anderson MS, Bull HS, Galloway SM, Kelly TM, Mohan S. et al. 1993. J. Biol. Chem. 268:19858–65 [Google Scholar]
  74. Kelly TM, Stachula SA, Raetz CRH, Anderson MS. 1993. J. Biol. Chem. 268:19866–74 [Google Scholar]
  75. Young K, Silver LL, Bramhill D, Cameron P, Eveland SS. et al. 1995. J. Biol. Chem. 270:30384–91 [Google Scholar]
  76. Radika K, Raetz CRH. 1988. J. Biol. Chem. 263:14859–67 [Google Scholar]
  77. Babinski KJ, Kanjilal SJ, Raetz CRH. 2002. J. Biol. Chem. 277:25947–56 [Google Scholar]
  78. Babinski KJ, Ribeiro AA, Raetz CRH. 2002. J. Biol. Chem. 277:25937–46 [Google Scholar]
  79. Garrett TA, Kadrmas JL, Raetz CRH. 1997. J. Biol. Chem. 272:21855–64 [Google Scholar]
  80. Clementz T, Bednarski JJ, Raetz CRH. 1996. J. Biol. Chem. 271:12095–102 [Google Scholar]
  81. Clementz T, Zhou Z, Raetz CRH. 1997. J. Biol. Chem. 272:10353–60 [Google Scholar]
  82. Carty SM, Sreekumar KR, Raetz CRH. 1999. J. Biol. Chem. 274:9677–85 [Google Scholar]
  83. Vorachek-Warren MK, Ramirez S, Cotter RJ, Raetz CRH. 2002. J. Biol. Chem. 277:14194–205 [Google Scholar]
  84. Liu D, Sun TP, Raetz CRH. 2003. FASEB J. 17:(Suppl. S, Pt. 1) A579 [Google Scholar]
  85. Armstrong MT, Theg SM, Braun N, Wainwright N, Pardy RL, Armstrong PB. 2006. FASEB J. 20:2145–46 [Google Scholar]
  86. Anderson MS, Raetz CRH. 1987. J. Biol. Chem. 262:5159–69 [Google Scholar]
  87. Williamson JM, Anderson MS, Raetz CRH. 1991. J. Bacteriol. 173:3591–96 [Google Scholar]
  88. Wyckoff TJO, Lin S, Cotter RJ, Dotson GD, Raetz CRH. 1998. J. Biol. Chem. 273:32369–72 [Google Scholar]
  89. Odegaard TJ, Kaltashov IA, Cotter RJ, Steeghs L, van der Ley P. et al. 1997. J. Biol. Chem. 272:19688–96 [Google Scholar]
  90. Sweet CR, Williams AH, Karbarz MJ, Werts C, Kalb SR. et al. 2004. J. Biol. Chem. 279:25411–19 [Google Scholar]
  91. Dotson GD, Kaltashov IA, Cotter RJ, Raetz CRH. 1998. J. Bacteriol. 180:330–37 [Google Scholar]
  92. Raetz CRH, Roderick SL. 1995. Science 270:997–1000 [Google Scholar]
  93. Lee BI, Suh SW. 2003. Proteins 53:772–74 [Google Scholar]
  94. Williams AH, Immormino RM, Gewirth DT, Raetz CRH. 2006. Proc. Natl. Acad. Sci. USA 103:10877–82 [Google Scholar]
  95. Wyckoff TJ, Raetz CRH. 1999. J. Biol. Chem. 274:27047–55 [Google Scholar]
  96. Weckesser J, Mayer H. 1988. FEMS Microbiol Rev 4:143–53 [Google Scholar]
  97. Sweet CR, Ribeiro AA, Raetz CRH. 2004. J. Biol. Chem. 279:25400–10 [Google Scholar]
  98. Que-Gewirth NLS, Ribeiro AA, Kalb SR, Cotter RJ, Bulach DM. et al. 2004. J. Biol. Chem. 279:25420–29 [Google Scholar]
  99. Anderson MS, Robertson AD, Macher I, Raetz CRH. 1988. Biochemistry 27:1908–17 [Google Scholar]
  100. Jackman JE, Raetz CRH, Fierke CA. 1999. Biochemistry 38:1902–11 [Google Scholar]
  101. Jackman JE, Raetz CRH, Fierke CA. 2001. Biochemistry 40:514–23 [Google Scholar]
  102. Jackman JE, Fierke CA, Tumey LN, Pirrung M, Uchiyama T. et al. 2000. J. Biol. Chem. 275:11002–9 [Google Scholar]
  103. Clements JM, Coignard F, Johnson I, Chandler S, Palan S. et al. 2002. Antimicrob. Agents Chemother. 46:1793–99 [Google Scholar]
  104. McClerren AL, Endsley S, Bowman JL, Andersen NH, Guan Z. et al. 2005. Biochemistry 44:16574–83 [Google Scholar]
  105. Whittington DA, Rusche KM, Shin H, Fierke CA, Christianson DW. 2003. Proc. Natl. Acad. Sci. USA 100:8146–50 [Google Scholar]
  106. Hernick M, Gennadios HA, Whittington DA, Rusche KM, Christianson DW, Fierke CA. 2005. J. Biol. Chem. 280:16969–78 [Google Scholar]
  107. Gennadios HA, Whittington DA, Li X, Fierke CA, Christianson DW. 2006. Biochemistry 45:7940–48 [Google Scholar]
  108. Gennadios HA, Christianson DW. 2006. Biochemistry 45:15216–23 [Google Scholar]
  109. Coggins BE, Li X, McClerren AL, Hindsgaul O, Raetz CRH, Zhou P. 2003. Nat. Struct. Biol. 10:645–51 [Google Scholar]
  110. Coggins BE, McClerren AL, Jiang L, Li X, Rudolph J. et al. 2005. Biochemistry 44:1114–26 [Google Scholar]
  111. Sorensen PG, Lutkenhaus J, Young K, Eveland SS, Anderson MS, Raetz CRH. 1996. J. Biol. Chem. 271:25898–905 [Google Scholar]
  112. Fuhrer F, Langklotz S, Narberhaus F. 2006. Mol. Microbiol. 59:1025–36 [Google Scholar]
  113. Ogura T, Inoue K, Tatsuta T, Suzaki T, Karata K. et al. 1999. Mol. Microbiol. 31:833–44 [Google Scholar]
  114. Buetow L, Smith TK, Dawson A, Fyffe S, Hunter WN. 2007. Proc. Natl. Acad. Sci. USA 104:4321–26 [Google Scholar]
  115. Hu Y, Chen L, Ha S, Gross B, Falcone B. et al. 2003. Proc. Natl. Acad. Sci. USA 100:845–49 [Google Scholar]
  116. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z. et al. 1997. Nucleic Acids Res. 25:3389–402 [Google Scholar]
  117. Haselberger A, Hildebrandt J, Lam C, Liehl E, Loibner H. et al. 1987. Triangle 26:33–49 [Google Scholar]
  118. Scholz D, Bednarik K, Ehn G, Neruda W, Janzek E. et al. 1992. J. Med. Chem. 35:2070–74 [Google Scholar]
  119. Albers U, Reus K, Shuman HA, Hilbi H. 2005. Microbiology 151:167–82 [Google Scholar]
  120. Garrett TA, Que NL, Raetz CRH. 1998. J. Biol. Chem. 273:12457–65 [Google Scholar]
  121. Belunis CJ, Raetz CRH. 1992. J. Biol. Chem. 267:9988–97 [Google Scholar]
  122. Clementz T, Raetz CRH. 1991. J. Biol. Chem. 266:9687–96 [Google Scholar]
  123. Brozek KA, Raetz CRH. 1990. J. Biol. Chem. 265:15410–17 [Google Scholar]
  124. Ray BL, Raetz CRH. 1987. J. Biol. Chem. 262:1122–28 [Google Scholar]
  125. Lien E, Means TK, Heine H, Yoshimura A, Kusumoto S. et al. 2000. J. Clin. Investig. 105:497–504 [Google Scholar]
  126. Poltorak A, Ricciardi-Castagnoli P, Citterio S, Beutler B. 2000. Proc. Natl. Acad. Sci. USA 97:2163–67 [Google Scholar]
  127. Saitoh S, Akashi S, Yamada T, Tanimura N, Kobayashi M. et al. 2004. Int. Immunol. 16:961–69 [Google Scholar]
  128. Brozek KA, Hosaka K, Robertson AD, Raetz CRH. 1989. J. Biol. Chem. 264:6956–66 [Google Scholar]
  129. Meredith TC, Woodard RW. 2003. J. Biol. Chem. 278:32771–77 [Google Scholar]
  130. Sperandeo P, Pozzi C, Deho G, Polissi A. 2006. Res. Microbiol. 157:547–58 [Google Scholar]
  131. White KA, Kaltashov IA, Cotter RJ, Raetz CRH. 1997. J. Biol. Chem. 272:16555–63 [Google Scholar]
  132. White KA, Lin S, Cotter RJ, Raetz CR. 1999. J. Biol. Chem. 274:31391–400 [Google Scholar]
  133. Brabetz W, Muller-Loennies S, Brade H. 2000. J. Biol. Chem. 275:34954–62 [Google Scholar]
  134. Isobe T, White KA, Allen AG, Peacock M, Raetz CRH, Maskell DJ. 1999. J. Bacteriol. 181:2648–51 [Google Scholar]
  135. Belunis CJ, Mdluli KE, Raetz CRH, Nano FE. 1992. J. Biol. Chem. 267:18702–7 [Google Scholar]
  136. Karow M, Georgopoulos C. 1992. J. Bacteriol. 174:702–10 [Google Scholar]
  137. Murray SR, Bermudes D, de Felipe KS, Low KB. 2001. J. Bacteriol. 183:5554–61 [Google Scholar]
  138. Somerville JJE, Cassiano L, Bainbridge B, Cunningham MD, Darveau RP. 1996. J. Clin. Investig. 97:359–65 [Google Scholar]
  139. Low KB, Ittensohn M, Le T, Platt J, Sodi S. et al. 1999. Nat. Biotechnol. 17:37–41 [Google Scholar]
  140. D’Hauteville H, Khan S, Maskell DJ, Kussak A, Weintraub A. et al. 2002. J. Immunol. 168:5240–51 [Google Scholar]
  141. Vorachek-Warren MK, Carty SM, Lin S, Cotter RJ, Raetz CRH. 2002. J. Biol. Chem. 277:14186–93 [Google Scholar]
  142. Montminy SW, Khan N, McGrath S, Walkowicz MJ, Sharp F. et al. 2006. Nat. Immunol. 7:1066–73 [Google Scholar]
  143. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W. 1998. Science 282:2215–20 [Google Scholar]
  144. Ferguson AD, Welte W, Hofmann E, Lindner B, Holst O. et al. 2000. Struct. Fold. Des. 8:585–92 [Google Scholar]
  145. Nishiyama K, Ikegami A, Moser M, Schiltz E, Tokuda H, Muller M. 2006. J. Biol. Chem. 281:35667–76 [Google Scholar]
  146. Steeghs L, den Hartog R, den Boer A, Zomer B, Roholl P, van der Ley P. 1998. Nature 392:449–50 [Google Scholar]
  147. Doerrler WT, Reedy MC, Raetz CRH. 2001. J. Biol. Chem. 276:11461–64 [Google Scholar]
  148. Karow M, Georgopoulos C. 1993. Mol. Microbiol. 7:69–79 [Google Scholar]
  149. Polissi A, Georgopoulos C. 1996. Mol. Microbiol. 20:1221–33 [Google Scholar]
  150. Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CRH. 1998. J. Biol. Chem. 273:12466–75 [Google Scholar]
  151. Chang G, Roth CB. 2001. Science 293:1793–800 [Google Scholar]
  152. Chang G. 2003. J. Mol. Biol. 330:419–30 [Google Scholar]
  153. Reyes CL, Chang G. 2005. Science 308:1028–31 [Google Scholar]
  154. Dawson RJ, Locher KP. 2006. Nature 443:180–85 [Google Scholar]
  155. Chang G, Roth CB, Reyes CL, Pornillos O, Chen YJ, Chen AP. 2006. Science 314:1875 [Google Scholar]
  156. Raetz CRH, Garrett TA, Reynolds CM, Shaw WA, Moore JD. et al. 2006. J. Lipid Res. 47:1097–11 [Google Scholar]
  157. Huijbregts RP, de Kroon AI, de Kruijff B. 1998. J. Biol. Chem. 273:18936–42 [Google Scholar]
  158. Doerrler WT, Raetz CRH. 2002. J. Biol. Chem. 277:36697–705 [Google Scholar]
  159. Kol MA, van Dalen A, de Kroon AI, de Kruijff B. 2003. J. Biol. Chem. 278:24586–93 [Google Scholar]
  160. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D. et al. 2004. Science 304:66–74 [Google Scholar]
  161. Osborn MJ, Rick PD, Rasmussen NS. 1980. J. Biol. Chem. 255:4246–51 [Google Scholar]
  162. Tefsen B, Bos MP, Beckers F, Tommassen J, de Cock H. 2005. J. Biol. Chem. 280:35961–66 [Google Scholar]
  163. Sperandeo P, Cescutti R, Villa R, Di Benedetto C, Candia D. et al. 2007. J. Bacteriol. 189:244–53 [Google Scholar]
  164. Braun M, Silhavy TJ. 2002. Mol. Microbiol. 45:1289–302 [Google Scholar]
  165. Borst P, Zelcer N, van Helvoort A. 2000. Biochim. Biophys. Acta 1486:128–44 [Google Scholar]
  166. Borst P, Elferink RO. 2002. Annu. Rev. Biochem. 71:537–92 [Google Scholar]
  167. Smit JJM, Schinkel AH, Oude Elferink RPJ, Groen AK, Wagenaar E. et al. 1993. Cell 75:451–62 [Google Scholar]
  168. Schmitz G, Liebisch G, Langmann T. 2006. FEBS Lett. 580:5597–610 [Google Scholar]
  169. Zhou Z, Lin S, Cotter RJ, Raetz CRH. 1999. J. Biol. Chem. 274:18503–14 [Google Scholar]
  170. Zhou Z, Ribeiro AA, Lin S, Cotter RJ, Miller SI, Raetz CRH. 2001. J. Biol. Chem. 276:43111–21 [Google Scholar]
  171. Brozek KA, Bulawa CE, Raetz CRH. 1987. J. Biol. Chem. 262:5170–79 [Google Scholar]
  172. Guo L, Lim KB, Poduje CM, Daniel M, Gunn JS. et al. 1998. Cell 95:189–98 [Google Scholar]
  173. Helander IM, Kilpeläinen I, Vaara M. 1994. Mol. Microbiol. 11:481–87 [Google Scholar]
  174. Nummila K, Kilpeläinen I, Zähringer U, Vaara M, Helander IM. 1995. Mol. Microbiol. 16:271–78 [Google Scholar]
  175. Helander IM, Kato Y, Kilpelainen I, Kostiainen R, Lindner B. et al. 1996. Eur. J. Biochem. 237:272–78 [Google Scholar]
  176. Breazeale SD, Ribeiro AA, Raetz CRH. 2002. J. Biol. Chem. 277:2886–96 [Google Scholar]
  177. Breazeale SD, Ribeiro AA, Raetz CRH. 2003. J. Biol. Chem. 279:24731–39 [Google Scholar]
  178. Breazeale SD, Ribeiro AA, McClerren AL, Raetz CRH. 2005. J. Biol. Chem. 280:14154–67 [Google Scholar]
  179. Williams GJ, Breazeale SD, Raetz CRH, Naismith JH. 2005. J. Biol. Chem. 280:23000–8 [Google Scholar]
  180. Gatzeva-Topalova PZ, May AP, Sousa MC. 2005. Structure 13:929–42 [Google Scholar]
  181. Noland BW, Newman JM, Hendle J, Badger J, Christopher JA. et al. 2002. Structure 10:1569–80 [Google Scholar]
  182. Gunn JS, Ryan SS, Van Velkinburgh JC, Ernst RK, Miller SI. 2000. Infect. Immun. 68:6139–46 [Google Scholar]
  183. Kanipes MI, Lin S, Cotter RJ, Raetz CRH. 2001. J. Biol. Chem. 276:1156–63 [Google Scholar]
  184. Figueroa-Bossi N, Lemire S, Maloriol D, Balbontin R, Casadesus J, Bossi L. 2006. Mol. Microbiol. 62:838–52 [Google Scholar]
  185. Tamayo R, Choudhury B, Septer A, Merighi M, Carlson R, Gunn JS. 2005. J. Bacteriol. 187:3391–99 [Google Scholar]
  186. Kim SH, Jia W, Parreira VR, Bishop RE, Gyles CL. 2006. Microbiology 152:657–66 [Google Scholar]
  187. Kim SH, Jia W, Bishop RE, Gyles C. 2004. Infect. Immun. 72:1174–80 [Google Scholar]
  188. Kaniuk NA, Vinogradov E, Li J, Monteiro MA, Whitfield C. 2004. J. Biol. Chem. 279:31237–50 [Google Scholar]
  189. El Ghachi M, Derbise A, Bouhss A, Mengin-Lecreulx D. 2005. J. Biol. Chem. 280:18689–95 [Google Scholar]
  190. Lazar K, Walker S. 2002. Curr. Opin. Chem. Biol. 6:786–93 [Google Scholar]
  191. Cho US, Bader MW, Amaya MF, Daley ME, Klevit RE. et al. 2006. J. Mol. Biol. 356:1193–206 [Google Scholar]
  192. Martin-Orozco N, Touret N, Zaharik ML, Park E, Kopelman R. et al. 2006. Mol. Biol. Cell 17:498–510 [Google Scholar]
  193. Winfield MD, Groisman EA. 2004. Proc. Natl. Acad. Sci. USA 101:17162–67 [Google Scholar]
  194. Guina T, Yi EC, Wang H, Hackett M, Miller SI. 2000. J. Bacteriol. 182:4077–86 [Google Scholar]
  195. Robey M, O’Connell W, Cianciotto NP. 2001. Infect. Immun. 69:4276–86 [Google Scholar]
  196. Preston A, Maxim E, Toland E, Pishko EJ, Harvill ET. et al. 2003. Mol. Microbiol. 48:725–36 [Google Scholar]
  197. Pilione MR, Pishko EJ, Preston A, Maskell DJ, Harvill ET. 2004. Infect. Immun. 72:2837–42 [Google Scholar]
  198. Bishop RE. 2005. Mol. Microbiol. 57:900–12 [Google Scholar]
  199. Rebeil R, Ernst RK, Gowen BB, Miller SI, Hinnebusch BJ. 2004. Mol. Microbiol. 52:1363–73 [Google Scholar]
  200. Ahn VE, Lo EI, Engel CK, Chen L, Hwang PM. et al. 2004. EMBO J. 23:2931–41 [Google Scholar]
  201. Hwang PM, Choy WY, Lo EI, Chen L, Forman-Kay JD. et al. 2002. Proc. Natl. Acad. Sci. USA 99:13560–65 [Google Scholar]
  202. Evanics F, Hwang PM, Cheng Y, Kay LE, Prosser RS. 2006. J. Am. Chem. Soc. 128:8256–64 [Google Scholar]
  203. Khan MA, Neale C, Michaux C, Pomès R, Privé GG. et al. 2007. Biochemistry 46:4565–79 [Google Scholar]
  204. Stover AG, Da Silva Correia J, Evans JT, Cluff CW, Elliott MW. et al. 2004. J. Biol. Chem. 279:4440–509 [Google Scholar]
  205. Hwang PM, Bishop RE, Kay LE. 2004. Proc. Natl. Acad. Sci. USA 101:9618–23 [Google Scholar]
  206. Tam C, Missiakas D. 2005. Mol. Microbiol. 55:1403–12 [Google Scholar]
  207. Gibbons HS, Lin S, Cotter RJ, Raetz CRH. 2000. J. Biol. Chem. 275:32940–49 [Google Scholar]
  208. Raetz CRH. 2001. J. Endotoxin Res. 7:73–78 [Google Scholar]
  209. Kawasaki K, Ernst RK, Miller SI. 2005. J. Bacteriol. 187:2448–57 [Google Scholar]
  210. Geurtsen J, Steeghs L, Hamstra HJ, Ten Hove J, de Haan A. et al. 2006. Infect. Immun. 74:5574–85 [Google Scholar]
  211. Kawasaki K, Ernst RK, Miller SI. 2004. J. Biol. Chem. 279:20044–48 [Google Scholar]
  212. Ernst RK, Adams KN, Moskowitz SM, Kraig GM, Kawasaki K. et al. 2006. J. Bacteriol. 188:191–201 [Google Scholar]
  213. Geurtsen J, Steeghs L, Hove JT, van der Ley P, Tommassen J. 2005. J. Biol. Chem. 280:8248–59 [Google Scholar]
  214. Rutten L, Geurtsen J, Lambert W, Smolenaers JJ, Bonvin AM. et al. 2006. Proc. Natl. Acad. Sci. USA 103:7071–76 [Google Scholar]
  215. Ellis J, Oyston PC, Green M, Titball RW. 2002. Clin. Microbiol. Rev. 15:631–46 [Google Scholar]
  216. Kieffer TL, Cowley S, Nano FE, Elkins KL. 2003. Microb. Infect. 5:397–403 [Google Scholar]
  217. Wang X, Ribeiro AA, Guan Z, McGrath S, Cotter R, Raetz CRH. 2006. Biochemistry 45:14427–40 [Google Scholar]
  218. Larsson P, Oyston PC, Chain P, Chu MC, Duffield M. et al. 2005. Nat. Genet. 37:153–59 [Google Scholar]
  219. Stead C, Tran A, Ferguson DJ, McGrath S, Cotter R, Trent S. 2005. J. Bacteriol. 187:3374–83 [Google Scholar]
  220. Phillips NJ, Schilling B, McLendon MK, Apicella MA, Gibson BW. 2004. Infect. Immun. 72:5340–48 [Google Scholar]
  221. Vinogradov E, Perry MB, Conlan JW. 2002. Eur. J. Biochem. 269:6112–18 [Google Scholar]
  222. Wang X, Ribeiro AA, Guan Z, Abraham SN, Raetz CRH. 2007. Proc. Natl. Acad. Sci. USA 104:4136–41 [Google Scholar]
  223. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG. et al. 1997. Nature 388:539–47 [Google Scholar]
  224. Bhat UR, Forsberg LS, Carlson RW. 1994. J. Biol. Chem. 269:14402–10 [Google Scholar]
  225. Que NLS, Lin S, Cotter RJ, Raetz CRH. 2000. J. Biol. Chem. 275:28006–16 [Google Scholar]
  226. Que NLS, Ribeiro AA, Raetz CRH. 2000. J. Biol. Chem. 275:28017–27 [Google Scholar]
  227. Bhat UR, Mayer H, Yokota A, Hollingsworth RI, Carlson R. 1991. J. Bacteriol. 173:2155–59 [Google Scholar]
  228. Basu SS, White KA, Que NL, Raetz CRH. 1999. J. Biol. Chem. 274:11150–58 [Google Scholar]
  229. Carlson RW, Reuhs B, Chen TB, Bhat UR, Noel KD. 1995. J. Biol. Chem. 270:11783–88 [Google Scholar]
  230. Brozek KA, Kadrmas JL, Raetz CRH. 1996. J. Biol. Chem. 271:32112–18 [Google Scholar]
  231. Price NPJ, Kelly TM, Raetz CRH, Carlson RW. 1994. J. Bacteriol. 176:4646–55 [Google Scholar]
  232. Basu SS, Karbarz MJ, Raetz CRH. 2002. J. Biol. Chem. 277:28959–71 [Google Scholar]
  233. Brozek KA, Carlson RW, Raetz CRH. 1996. J. Biol. Chem. 271:32126–36 [Google Scholar]
  234. Karbarz MJ, Kalb SR, Cotter RJ, Raetz CRH. 2003. J. Biol. Chem. 278:39269–79 [Google Scholar]
  235. Que-Gewirth NLS, Lin S, Cotter RJ, Raetz CRH. 2003. J. Biol. Chem. 278:12109–19 [Google Scholar]
  236. Que-Gewirth NLS, Karbarz MJ, Kalb SR, Cotter RJ, Raetz CRH. 2003. J. Biol. Chem. 278:12120–29 [Google Scholar]
  237. Kanjilal-Kolar S, Basu SS, Kanipes MI, Guan Z, Garrett TA, Raetz CRH. 2006. J. Biol. Chem. 281:12865–78 [Google Scholar]
  238. Kanjilal-Kolar S, Raetz CRH. 2006. J. Biol. Chem. 281:12879–87 [Google Scholar]
  239. Ferguson GP, Datta A, Carlson RW, Walker GC. 2005. Mol. Microbiol. 56:68–80 [Google Scholar]
  240. Vedam V, Kannenberg EL, Haynes JG, Sherrier DJ, Datta A, Carlson RW. 2003. J. Bacteriol. 185:1841–50 [Google Scholar]
  241. Boon Hinckley M, Reynolds CM, Ribeiro AA, McGrath SC, Cotter RJ. et al. 2005. J. Biol. Chem. 280:30214–24 [Google Scholar]
  242. Vinogradov EV, Muller-Loennies S, Petersen BO, Meshkov S, Thomas-Oates JE. et al. 1997. Eur. J. Biochem. 247:82–90 [Google Scholar]
  243. Bode CE, Brabetz W, Brade H. 1998. Eur. J. Biochem. 254:404–12 [Google Scholar]
  244. Schneider JE, Reinhold V, Rumley MK, Kennedy EP. 1979. J. Biol. Chem. 254:10135–38 [Google Scholar]
  245. Kennedy EP. 1987. In Escherichia coli and Salmonella typhimurium ed. FC Neidhardt pp. 672–79 Vol I. Washington, DC: ASM Publ. [Google Scholar]
  246. Wu HC. 1996. In Escherichia coli and Salmonella: Cellular and Molecular Biology ed. FC Neidhardt pp. 1005–14 Washington, DC: Am. Soc. Microbiol. [Google Scholar]
  247. Raetz CRH. 1986. Annu. Rev. Genet. 20:253–95 [Google Scholar]
  248. Cronan JE. 2003. Annu. Rev. Microbiol. 57:203–24 [Google Scholar]
  249. Stevenson G, Neal B, Liu D, Hobbs M, Packer NH. et al. 1994. J. Bacteriol. 176:4144–56 [Google Scholar]
  250. Murphy RC, Raetz CRH, Reynolds CM, Barkley RM. 2005. Prostaglandins Other Lipid Mediat. 77:131–40 [Google Scholar]
  251. Jain NU, Wyckoff TJ, Raetz CRH, Prestegard JH. 2004. J. Mol. Biol. 343:1379–89 [Google Scholar]
  252. Feldman MF, Marolda CL, Monteiro MA, Perry MB, Parodi AJ, Valvano MA. 1999. J. Biol. Chem. 274:35129–38 [Google Scholar]
  253. Strain SM, Armitage IM, Anderson L, Takayama K, Qureshi N, Raetz CRH. 1985. J. Biol. Chem. 260:16089–98 [Google Scholar]
  254. Zhou Z, Ribeiro AA, Raetz CRH. 2000. J. Biol. Chem. 275:13542–51 [Google Scholar]
  255. Price NJP, Jeyaretnam B, Carlson RW, Kadrmas JL, Raetz CRH, Brozek KA. 1995. Proc. Natl. Acad. Sci. USA 92:7352–56 [Google Scholar]
  256. Kadrmas JL, Brozek KA, Raetz CRH. 1996. J. Biol. Chem. 271:32119–25 [Google Scholar]
  257. Kadrmas JL, Allaway D, Studholme RE, Sullivan JT, Ronson CW. et al. 1998. J. Biol. Chem. 273:26432–40 [Google Scholar]
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Lipid A Modification Systems in Gram-Negative Bacteria
Annual Review of Biochemistry 76, 295 (2007); https://doi.org/10.1146/annurev.biochem.76.010307.145803
/content/journals/10.1146/annurev.biochem.76.010307.145803
/content/journals/10.1146/annurev.biochem.76.010307.145803
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