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Abstract

Lipoteichoic acid (LTA) is an important cell wall polymer found in gram-positive bacteria. Although the exact role of LTA is unknown, mutants display significant growth and physiological defects. Additionally, modification of the LTA backbone structure can provide protection against cationic antimicrobial peptides. This review provides an overview of the different LTA types and their chemical structures and synthesis pathways. The occurrence and mechanisms of LTA modifications with -alanyl, glycosyl, and phosphocholine residues will be discussed along with their functions. Similarities between the production of type I LTA and osmoregulated periplasmic glucans in gram-negative bacteria are highlighted, indicating that LTA should perhaps be compared to these polymers rather than lipopolysaccharide, as is presently the case. Lastly, current efforts to use LTAs as vaccine candidates, synthesis proteins as novel antimicrobial targets, and LTA mutant strains as improved probiotics are highlighted.

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An erratum has been published for this article:
Lipoteichoic Acid Synthesis and Function in Gram-Positive Bacteria
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2014-09-08
2024-06-23
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Literature Cited

  1. Abachin E, Poyart C, Pellegrini E, Milohanic E, Fiedler F. 1.  et al. 2002. Formation of d-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43:1–14 [Google Scholar]
  2. Abi Khattar Z, Rejasse A, Destoumieux-Garzón D, Escoubas JM, Sanchis V. 2.  et al. 2009. The dlt operon of Bacillus cereus is required for resistance to cationic antimicrobial peptides and for virulence in insects. J. Bacteriol. 191:7063–73 [Google Scholar]
  3. Alderwick LJ, Lloyd GS, Ghadbane H, May JW, Bhatt A. 3.  et al. 2011. The C-terminal domain of the arabinosyltransferase Mycobacterium tuberculosis EmbC is a lectin-like carbohydrate binding module. PLoS Pathog. 7:e1001299 [Google Scholar]
  4. Arakawa H, Shimada A, Ishimoto N, Ito E. 4.  1981. Occurrence of ribitol-containing lipoteichoic acid in Staphylococcus aureus H and its glycosylation. J. Biochem. 89:1555–63 [Google Scholar]
  5. Archibald AR, Baddiley J, Heptinstall S. 5.  1973. The alanine ester content and magnesium binding capacity of walls of Staphylococcus aureus H grown at different pH values. Biochim. Biophys. Acta 291:629–34 [Google Scholar]
  6. Armstrong JJ, Baddiley J, Buchanan JG, Davision AL, Kelemen MV, Neuhaus FC. 6.  1958. Isolation and structure of ribitol phosphate derivatives (teichoic acids) from bacterial cell walls. J. Chem. Soc. 1958:4344–54 [Google Scholar]
  7. Armstrong JJ, Baddiley J, Buchanan JG, Davision AL, Kelemen MV, Neuhaus FC. 7.  1959. Composition of teichoic acids from a number of bacterial walls. Nature 184:247–48 [Google Scholar]
  8. Baddiley J. 8.  1972. Teichoic acids in cell walls and membranes of bacteria. Essays Biochem. 8:35–77 [Google Scholar]
  9. Bai Y, Yang J, Zarrella TM, Zhang Y, Metzger DW, Bai G. 9.  2013. Cyclic di-AMP impairs potassium uptake mediated by a cyclic di-AMP binding protein in Streptococcus pneumoniae. J. Bacteriol. 196:614–23 [Google Scholar]
  10. Baur S, Marles-Wright J, Buckenmaier S, Lewis RJ, Vollmer W. 10.  2009. Synthesis of CDP-activated ribitol for teichoic acid precursors in Streptococcus pneumoniae. J. Bacteriol. 191:1200–10 [Google Scholar]
  11. Berg S, Kaur D, Jackson M, Brennan PJ. 11.  2007. The glycosyltransferases of Mycobacterium tuberculosis—roles in the synthesis of arabinogalactan, lipoarabinomannan, and other glycoconjugates. Glycobiology 17:35R–56R [Google Scholar]
  12. Bergström N, Jansson PE, Kilian M, Skov Sørensen UB. 12.  2000. Structures of two cell wall-associated polysaccharides of a Streptococcus mitis biovar 1 strain: a unique teichoic acid-like polysaccharide and the group O antigen which is a C-polysaccharide in common with pneumococci. Eur. J. Biochem. 267:7147–57 [Google Scholar]
  13. Bertolo L, Boncheff AG, Ma Z, Chen YH, Wakeford T. 13.  et al. 2012. Clostridium difficile carbohydrates: glucan in spores, PSII common antigen in cells, immunogenicity of PSII in swine and synthesis of a dual C. difficile–ETEC conjugate vaccine. Carbohydr. Res. 354:79–86 [Google Scholar]
  14. Bhagwat AA, Jun W, Liu L, Kannan P, Dharne M. 14.  et al. 2009. Osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium are required for optimal virulence in mice. Microbiology 155:229–37 [Google Scholar]
  15. Bontemps-Gallo S, Cogez V, Robbe-Masselot C, Quintard K, Dondeyne J. 15.  et al. 2013. Biosynthesis of osmoregulated periplasmic glucans in Escherichia coli: The phosphoethanolamine transferase is encoded by opgE. BioMed. Res. Int. 2013:371429 [Google Scholar]
  16. Breazeale SD, Ribeiro AA, McClerren AL, Raetz CR. 16.  2005. A formyltransferase required for polymyxin resistance in Escherichia coli and the modification of lipid A with 4-amino-4-deoxy-l-arabinose: identification and function of UDP-4-deoxy-4-formamido-l-arabinose. J. Biol. Chem. 280:14154–67 [Google Scholar]
  17. Brown S, Santa Maria JP Jr, Walker S. 17.  2013. Wall teichoic acids of gram-positive bacteria. Annu. Rev. Microbiol. 67:313–36 [Google Scholar]
  18. Chen Q, Dintaman J, Lees A, Sen G, Schwartz D. 18.  et al. 2013. Novel synthetic (poly)glycerolphosphate-based antistaphylococcal conjugate vaccine. Infect. Immun. 81:2554–61 [Google Scholar]
  19. Chien AC, Zareh SK, Wang YM, Levin PA. 19.  2012. Changes in the oligomerization potential of the division inhibitor UgtP co-ordinate Bacillus subtilis cell size with nutrient availability. Mol. Microbiol. 86:594–610 [Google Scholar]
  20. Childs WC III, Neuhaus FC. 20.  1980. Biosynthesis of d-alanyl-lipoteichoic acid: characterization of ester-linked d-alanine in the in vitro-synthesized product. J. Bacteriol. 143:293–301 [Google Scholar]
  21. Collins LV, Kristian SA, Weidenmaier C, Faigle M, Van Kessel KP. 21.  et al. 2002. Staphylococcus aureus strains lacking d-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J. Infect. Dis. 186:214–19 [Google Scholar]
  22. Corrigan RM, Abbott JC, Burhenne H, Kaever V, Gründling A. 22.  2011. c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog. 7:e1002217 [Google Scholar]
  23. Corrigan RM, Campeotto I, Jeganathan T, Roelofs KG, Lee VT, Gründling A. 23.  2013. Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc. Natl. Acad. Sci. USA 110:9084–89 [Google Scholar]
  24. Corrigan RM, Gründling A. 24.  2013. Cyclic di-AMP: another second messenger enters the fray. Nat. Rev. Microbiol. 11:513–24 [Google Scholar]
  25. Cox AD, St. Michael F, Aubry A, Cairns CM, Strong PC. 25.  et al. 2013. Investigating the candidacy of a lipoteichoic acid-based glycoconjugate as a vaccine to combat Clostridium difficile infection. Glycoconj. J. 30:843–55 [Google Scholar]
  26. Damjanovic M, Kharat AS, Eberhardt A, Tomasz A, Vollmer W. 26.  2007. The essential tacF gene is responsible for the choline-dependent growth phenotype of Streptococcus pneumoniae. J. Bacteriol. 189:7105–11 [Google Scholar]
  27. Debabov DV, Kiriukhin MY, Neuhaus FC. 27.  2000. Biosynthesis of lipoteichoic acid in Lactobacillus rhamnosus: role of DltD in d-alanylation. J. Bacteriol. 182:2855–64 [Google Scholar]
  28. Dehus O, Pfitzenmaier M, Stuebs G, Fischer N, Schwaeble W. 28.  et al. 2011. Growth temperature-dependent expression of structural variants of Listeria monocytogenes lipoteichoic acid. Immunobiology 216:24–31 [Google Scholar]
  29. Denapaite D, Brückner R, Hakenbeck R, Vollmer W. 29.  2012. Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species: lessons from genomes. Microb. Drug Resist. 18:344–58 [Google Scholar]
  30. Du L, He Y, Luo Y. 30.  2008. Crystal structure and enantiomer selection by d-alanyl carrier protein ligase DltA from Bacillus cereus. Biochemistry 47:11473–80 [Google Scholar]
  31. Eberhardt A, Wu LJ, Errington J, Vollmer W, Veening JW. 31.  2009. Cellular localization of choline-utilization proteins in Streptococcus pneumoniae using novel fluorescent reporter systems. Mol. Microbiol. 74:395–408 [Google Scholar]
  32. Fabretti F, Theilacker C, Baldassarri L, Kaczynski Z, Kropec A. 32.  et al. 2006. Alanine esters of enterococcal lipoteichoic acid play a role in biofilm formation and resistance to antimicrobial peptides. Infect. Immun. 74:4164–71 [Google Scholar]
  33. Fischer W. 33.  1990. Bacterial phosphoglycolipids and lipoteichoic acids. Handbook of Lipid Research D Hanahan 123–234 New York: Plenum [Google Scholar]
  34. Fischer W. 34.  1994. Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus. Med. Microbiol. Immunol. 183:61–76 [Google Scholar]
  35. Fischer W. 35.  1994. Lipoteichoic acids and lipoglycans. Bacterial Cell Wall JM Ghuysen, R Hackenbeck 199–214 Amsterdam: Elsevier Science [Google Scholar]
  36. Fischer W. 36.  2000. Phosphocholine of pneumococcal teichoic acids: role in bacterial physiology and pneumococcal infection. Res. Microbiol. 151:421–27 [Google Scholar]
  37. Fischer W, Rösel P. 37.  1980. The alanine ester substitution of lipoteichoic acid (LTA) in Staphylococcus aureus. FEBS Lett. 119:224–26 [Google Scholar]
  38. Gárcia JL, Sánchez-Beato AR, Medrano FJ, López R. 38.  1998. Versatility of choline-binding domain. Microb. Drug Resist. 4:25–36 [Google Scholar]
  39. Garufi G, Hendrickx AP, Beeri K, Kern JW, Sharma A. 39.  et al. 2012. Synthesis of lipoteichoic acids in Bacillus anthracis. J. Bacteriol. 194:4312–21 [Google Scholar]
  40. Gisch N, Kohler T, Ulmer AJ, Müthing J, Pribyl T. 40.  et al. 2013. Structural reevaluation of Streptococcus pneumoniae lipoteichoic acid and new insights into its immunostimulatory potency. J. Biol. Chem. 288:15654–67 [Google Scholar]
  41. Goebel WF, Adams MH. 41.  1943. The immunological properties of the heterophile antigen and somatic polysaccharide of pneumococcus. J. Exp. Med. 77:435–49 [Google Scholar]
  42. Goldberg DE, Rumley MK, Kennedy EP. 42.  1981. Biosynthesis of membrane-derived oligosaccharides: a periplasmic phosphoglyceroltransferase. Proc. Natl. Acad. Sci. USA 78:5513–17 [Google Scholar]
  43. Gründling A, Schneewind O. 43.  2007. Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus. J. Bacteriol. 189:2521–30 [Google Scholar]
  44. Gründling A, Schneewind O. 44.  2007. Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 104:8478–83 [Google Scholar]
  45. Hankins JV, Madsen JA, Giles DK, Brodbelt JS, Trent MS. 45.  2012. Amino acid addition to Vibrio cholerae LPS establishes a link between surface remodeling in gram-positive and gram-negative bacteria. Proc. Natl. Acad. Sci. USA 109:8722–27 [Google Scholar]
  46. Heaton MP, Neuhaus FC. 46.  1992. Biosynthesis of d-alanyl-lipoteichoic acid: cloning, nucleotide sequence, and expression of the Lactobacillus casei gene for the d-alanine-activating enzyme. J. Bacteriol. 174:4707–17 [Google Scholar]
  47. Hermoso JA, Lagartera L, González A, Stelter M, García P. 47.  et al. 2005. Insights into pneumococcal pathogenesis from the crystal structure of the modular teichoic acid phosphorylcholine esterase Pce. Nat. Struct. Mol. Biol. 12:533–38 [Google Scholar]
  48. Hether NW, Jackson LL. 48.  1983. Lipoteichoic acid from Listeria monocytogenes. J. Bacteriol. 156:809–17 [Google Scholar]
  49. Hill NS, Buske PJ, Shi Y, Levin PA. 49.  2013. A moonlighting enzyme links Escherichia coli cell size with central metabolism. PLoS Genet. 9:e1003663 [Google Scholar]
  50. Hofmann K. 50.  2000. A superfamily of membrane-bound O-acyltransferases with implications for Wnt signaling. Trends Biochem. Sci. 25:111–12 [Google Scholar]
  51. Hurst A, Hughes A, Duckworth M, Baddiley J. 51.  1975. Loss of d-alanine during sublethal heating of Staphylococcus aureus S6 and magnesium binding during repair. J. Gen. Microbiol. 89:277–84 [Google Scholar]
  52. Icho T. 52.  1988. Membrane-bound phosphatases in Escherichia coli: sequence of the pgpB gene and dual subcellular localization of the pgpB product. J. Bacteriol. 170:5117–24 [Google Scholar]
  53. Icho T, Raetz CR. 53.  1983. Multiple genes for membrane-bound phosphatases in Escherichia coli and their action on phospholipid precursors. J. Bacteriol. 153:722–30 [Google Scholar]
  54. Iwasaki H, Shimada A, Ito E. 54.  1986. Comparative studies of lipoteichoic acids from several Bacillus strains. J. Bacteriol. 167:508–16 [Google Scholar]
  55. Iwasaki H, Shimada A, Yokoyama K, Ito E. 55.  1989. Structure and glycosylation of lipoteichoic acids in Bacillus strains. J. Bacteriol. 171:424–29 [Google Scholar]
  56. Jackson BJ, Bohin JP, Kennedy EP. 56.  1984. Biosynthesis of membrane-derived oligosaccharides: characterization of mdoB mutants defective in phosphoglycerol transferase I activity. J. Bacteriol. 160:976–81 [Google Scholar]
  57. Jerga A, Lu YJ, Schujman GE, de Mendoza D, Rock CO. 57.  2007. Identification of a soluble diacylglycerol kinase required for lipoteichoic acid production in Bacillus subtilis. J. Biol. Chem. 282:21738–45 [Google Scholar]
  58. Jerga A, Miller DJ, White SW, Rock CO. 58.  2009. Molecular determinants for interfacial binding and conformational change in a soluble diacylglycerol kinase. J. Biol. Chem. 284:7246–54 [Google Scholar]
  59. Jorasch P, Warnecke DC, Lindner B, Zähringer U, Heinz E. 59.  2000. Novel processive and nonprocessive glycosyltransferases from Staphylococcus aureus and Arabidopsis thaliana synthesize glycoglycerolipids, glycophospholipids, glycosphingolipids and glycosylsterols. Eur. J. Biochem. 267:3770–83 [Google Scholar]
  60. Jorasch P, Wolter FP, Zähringer U, Heinz E. 60.  1998. A UDP glucosyltransferase from Bacillus subtilis successively transfers up to four glucose residues to 1,2-diacylglycerol: expression of ypfP in Escherichia coli and structural analysis of its reaction products. Mol. Microbiol. 29:419–30 [Google Scholar]
  61. Karatsa-Dodgson M, Wörmann ME, Gründling A. 61.  2010. In vitro analysis of the Staphylococcus aureus lipoteichoic acid synthase enzyme using fluorescently labeled lipids. J. Bacteriol. 192:5341–49 [Google Scholar]
  62. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S. 62.  et al. 2011. A widespread family of bacterial cell wall assembly proteins. EMBO J. 30:4931–41 [Google Scholar]
  63. Kennedy EP. 63.  1996. Membrane-derived oligosaccharides (periplasmic β-d-glucans) of Escherichia coli. In Escherichia coli and Salmonella, ed. FC Neidhardt 1064–71 Washington, DC: ASM [Google Scholar]
  64. Kharat AS, Tomasz A. 64.  2006. Drastic reduction in the virulence of Streptococcus pneumoniae expressing type 2 capsular polysaccharide but lacking choline residues in the cell wall. Mol. Biol. 60:93–107 [Google Scholar]
  65. Khazaie K, Zadeh M, Khan MW, Bere P, Gounari F. 65.  et al. 2012. Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc. Natl. Acad. Sci. USA 109:10462–67 [Google Scholar]
  66. Kiriukhin MY, Debabov DV, Shinabarger DL, Neuhaus FC. 66.  2001. Biosynthesis of the glycolipid anchor in lipoteichoic acid of Staphylococcus aureus RN4220: role of YpfP, the diglucosyldiacylglycerol synthase. J. Bacteriol. 183:3506–14 [Google Scholar]
  67. Knox KW, Wicken AJ. 67.  1973. Immunological properties of teichoic acids. Bacteriol. Rev. 37:215–57 [Google Scholar]
  68. Koch HU, Fischer W. 68.  1978. Acyldiglucosyldiacylglycerol-containing lipoteichoic acid with a poly(3-O-galabiosyl-2-O-galactosyl-sn-glycero-1-phosphate) chain from Streptococcus lactis Kiel 42172. Biochemistry 17:5275–81 [Google Scholar]
  69. Koch HU, Haas R, Fischer W. 69.  1984. The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylococcus aureus. Eur. J. Biochem. 138:357–63 [Google Scholar]
  70. Koprivnjak T, Mlakar V, Swanson L, Fournier B, Peschel A, Weiss JP. 70.  2006. Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus. J. Bacteriol. 188:3622–30 [Google Scholar]
  71. Kovács M, Halfmann A, Fedtke I, Heintz M, Peschel A. 71.  et al. 2006. A functional dlt operon, encoding proteins required for incorporation of d-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J. Bacteriol. 188:5797–805 [Google Scholar]
  72. Kristian SA, Datta V, Weidenmaier C, Kansal R, Fedtke I. 72.  et al. 2005. d-Alanylation of teichoic acids promotes group A Streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J. Bacteriol. 187:6719–25 [Google Scholar]
  73. Lairson LL, Henrissat B, Davies GJ, Withers SG. 73.  2008. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77:521–55 [Google Scholar]
  74. Lequette Y, Lanfroy E, Cogez V, Bohin JP, Lacroix JM. 74.  2008. Biosynthesis of osmoregulated periplasmic glucans in Escherichia coli: The membrane-bound and the soluble periplasmic phosphoglycerol transferases are encoded by the same gene. Microbiology 154:476–83 [Google Scholar]
  75. Lightfoot YL, Mohamadzadeh M. 75.  2013. Tailoring gut immune responses with lipoteichoic acid-deficient Lactobacillus acidophilus. Front. Immunol. 4:25 [Google Scholar]
  76. Liu J, Mushegian A. 76.  2003. Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci. 12:1418–31 [Google Scholar]
  77. Lu D, Wörmann ME, Zhang X, Schneewind O, Gründling A, Freemont PS. 77.  2009. Structure-based mechanism of lipoteichoic acid synthesis by Staphylococcus aureus LtaS. Proc. Natl. Acad. Sci. USA 106:1584–89 [Google Scholar]
  78. Lu YH, Guan Z, Zhao J, Raetz CR. 78.  2011. Three phosphatidylglycerol-phosphate phosphatases in the inner membrane of Escherichia coli. J. Biol. Chem. 286:5506–18 [Google Scholar]
  79. MacArthur AE, Archibald AR. 79.  1984. Effect of culture pH on the d-alanine ester content of lipoteichoic acid in Staphylococcus aureus. J. Bacteriol. 160:792–93 [Google Scholar]
  80. Maestro B, González A, García P, Sanz JM. 80.  2007. Inhibition of pneumococcal choline-binding proteins and cell growth by esters of bicyclic amines. FEBS J. 274:364–76 [Google Scholar]
  81. Mancuso DJ, Chiu TH. 81.  1982. Biosynthesis of glucosyl monophosphoryl undecaprenol and its role in lipoteichoic acid biosynthesis. J. Bacteriol. 152:616–25 [Google Scholar]
  82. Mann B, Orihuela C, Antikainen J, Gao G, Sublett J. 82.  et al. 2006. Multifunctional role of choline binding protein G in pneumococcal pathogenesis. Infect. Immun. 74:821–29 [Google Scholar]
  83. Martín NS, Retamosa MG, Maestro B, Bartual SG, Rodes MJ. 83.  et al. 2013. Crystal structures of CbpF complexed with atropine and ipratropium reveal clues for the design of novel antimicrobials against Streptococcus pneumoniae. Biochim. Biophys. Acta 1840:129–35 [Google Scholar]
  84. Matias VR, Beveridge TJ. 84.  2005. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol. 56:240–51 [Google Scholar]
  85. Matias VR, Beveridge TJ. 85.  2006. Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J. Bacteriol. 188:1011–21 [Google Scholar]
  86. Matias VR, Beveridge TJ. 86.  2008. Lipoteichoic acid is a major component of the Bacillus subtilis periplasm. J. Bacteriol. 190:7414–18 [Google Scholar]
  87. Matsuoka S, Hashimoto M, Kamiya Y, Miyazawa T, Ishikawa K. 87.  et al. 2011. The Bacillus subtilis essential gene dgkB is dispensable in mutants with defective lipoteichoic acid synthesis. Genes Genet. Syst. 86:365–76 [Google Scholar]
  88. May JJ, Finking R, Wiegeshoff F, Weber TT, Bandur N. 88.  et al. 2005. Inhibition of the d-alanine: d-Alanyl carrier protein ligase from Bacillus subtilis increases the bacterium's susceptibility to antibiotics that target the cell wall. FEBS J. 272:2993–3003 [Google Scholar]
  89. McCormick NE, Halperin SA, Lee SF. 89.  2011. Regulation of d-alanylation of lipoteichoic acid in Streptococcus gordonii. Microbiology 157:2248–56 [Google Scholar]
  90. Miller DJ, Jerga A, Rock CO, White SW. 90.  2008. Analysis of the Staphylococcus aureus DgkB structure reveals a common catalytic mechanism for the soluble diacylglycerol kinases. Structure 16:1036–46 [Google Scholar]
  91. Mohamadzadeh M, Pfeiler EA, Brown JB, Zadeh M, Gramarossa M. 91.  et al. 2011. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc. Natl. Acad. Sci. USA 108:Suppl. 14623–30 [Google Scholar]
  92. Molina R, González A, Stelter M, Pérez-Dorado I, Kahn R. 92.  et al. 2009. Crystal structure of CbpF, a bifunctional choline-binding protein and autolysis regulator from Streptococcus pneumoniae. EMBO Rep. 10:246–51 [Google Scholar]
  93. Mukerji R, Mirza S, Roche AM, Widener RW, Croney CM. 93.  et al. 2012. Pneumococcal surface protein A inhibits complement deposition on the pneumococcal surface by competing with the binding of C-reactive protein to cell-surface phosphocholine. J. Immunobiol. 189:5327–35 [Google Scholar]
  94. Nelson JW, Sudarsan N, Furukawa K, Weinberg Z, Wang JX, Breaker RR. 94.  2013. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat. Chem. Biol. 9:834–39 [Google Scholar]
  95. Neuhaus FC, Baddiley J. 95.  2003. A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67:686–723 [Google Scholar]
  96. Ogunniyi AD, LeMessurier KS, Graham RM, Watt JM, Briles DE. 96.  et al. 2007. Contributions of pneumolysin, pneumococcal surface protein A (PspA), and PspC to pathogenicity of Streptococcus pneumoniae D39 in a mouse model. Infect. Immunol. 75:1843–51 [Google Scholar]
  97. Oku Y, Kurokawa K, Matsuo M, Yamada S, Lee BL, Sekimizu K. 97.  2009. Pleiotropic roles of polyglycerolphosphate synthase of lipoteichoic acid in growth of Staphylococcus aureus cells. J. Bacteriol. 191:141–51 [Google Scholar]
  98. Osman KT, Du L, He Y, Luo Y. 98.  2009. Crystal structure of Bacillus cereusd-alanyl carrier protein ligase (DltA) in complex with ATP. J. Mol. Biol. 388:345–55 [Google Scholar]
  99. Perea Vélez M, Verhoeven TL, Draing C, Von Aulock S, Pfitzenmaier M. 99.  et al. 2007. Functional analysis of d-alanylation of lipoteichoic acid in the probiotic strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 73:3595–604 [Google Scholar]
  100. Perego M, Glaser P, Minutello A, Strauch MA, Leopold K, Fischer W. 100.  1995. Incorporation of d-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J. Biol. Chem. 270:15598–606 [Google Scholar]
  101. Pérez-Dorado I, González A, Morales M, Sanles R, Striker W. 101.  et al. 2010. Insights into pneumococcal fratricide from the crystal structures of the modular killing factor LytC. Nat. Struct. Mol. Biol. 17:576–81 [Google Scholar]
  102. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Gotz F. 102.  1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405–10 [Google Scholar]
  103. Poyart C, Lamy MC, Boumaila C, Fiedler F, Trieu-Cuot P. 103.  2001. Regulation of d-alanyl-lipoteichoic acid biosynthesis in Streptococcus agalactiae involves a novel two-component regulatory system. J. Bacteriol. 183:6324–34 [Google Scholar]
  104. Reichmann NT, Cassona CP, Gründling A. 104.  2013. Revised mechanism of d-alanine incorporation into cell wall polymers in gram-positive bacteria. Microbiology 159:1868–77 [Google Scholar]
  105. Reichmann NT, Cassona CP, Monteiro JM, Bottomley AL, Corrigan RM. 105.  et al. 2014. Differential localization of LTA synthesis proteins and their interaction with the cell division machinery in Staphylococcus aureus. Mol. Microbiol. 92273–86
  106. Reichmann NT, Gründling A. 106.  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 [Google Scholar]
  107. Reid CW, Vinogradov E, Li J, Jarrell HC, Logan SM, Brisson JR. 107.  2012. Structural characterization of surface glycans from Clostridium difficile. Carbohydr. Res. 354:65–73 [Google Scholar]
  108. Richter SG, Elli D, Kim HK, Hendrickx AP, Sorg JA. 108.  et al. 2013. Small molecule inhibitor of lipoteichoic acid synthesis is an antibiotic for gram-positive bacteria. Proc. Natl. Acad. Sci. USA 110:3531–36 [Google Scholar]
  109. Saar-Dover R, Bitler A, Nezer R, Shmuel-Galia L, Firon A. 109.  et al. 2012. d-Alanylation of lipoteichoic acids confers resistance to cationic peptides in group B Streptococcus by increasing the cell wall density. PLoS Pathog. 8:e1002891 [Google Scholar]
  110. Schirner K, Marles-Wright J, Lewis RJ, Errington J. 110.  2009. Distinct and essential morphogenic functions for wall- and lipo-teichoic acids in Bacillus subtilis. EMBO J. 28:830–42 [Google Scholar]
  111. Seo HS, Cartee RT, Pritchard DG, Nahm MH. 111.  2008. A new model of pneumococcal lipoteichoic acid structure resolves biochemical, biosynthetic, and serologic inconsistencies of the current model. J. Bacteriol. 190:2379–87 [Google Scholar]
  112. Shindou H, Hishikawa D, Harayama T, Yuki K, Shimizu T. 112.  2009. Recent progress on acyl CoA: lysophospholipid acyltransferase research. J. Lipid Res. 50:Suppl.S46–51 [Google Scholar]
  113. Steen A, Palumbo E, Deghorain M, Cocconcelli PS, Delcour J. 113.  et al. 2005. Autolysis of Lactococcus lactis is increased upon d-alanine depletion of peptidoglycan and lipoteichoic acids. J. Bacteriol. 187:114–24 [Google Scholar]
  114. Stortz CA, Cherniak R, Jones RG, Treber TD, Reinhardt DJ. 114.  1990. Polysaccharides from Peptostreptococcus anaerobius and structure of the species-specific antigen. Carbohydr. Res. 207:101–20 [Google Scholar]
  115. Suntharalingam P, Senadheera MD, Mair RW, Lévesque CM, Cvitkovitch DG. 115.  2009. The LiaFSR system regulates the cell envelope stress response in Streptococcus mutans. J. Bacteriol. 191:2973–84 [Google Scholar]
  116. Taron DJ, Childs WC III, Neuhaus FC. 116.  1983. Biosynthesis of d-alanyl-lipoteichoic acid: role of diglyceride kinase in the synthesis of phosphatidylglycerol for chain elongation. J. Bacteriol. 154:1110–16 [Google Scholar]
  117. Theilacker C, Kaczynski Z, Kropec A, Fabretti F, Sange T. 117.  et al. 2006. Opsonic antibodies to Enterococcus faecalis strain 12030 are directed against lipoteichoic acid. Infec. Immun. 74:5703–12 [Google Scholar]
  118. Theilacker C, Kropec A, Hammer F, Sava I, Wobser D. 118.  et al. 2012. Protection against Staphylococcus aureus by antibody to the polyglycerolphosphate backbone of heterologous lipoteichoic acid. J. Infect. Dis. 205:1076–85 [Google Scholar]
  119. Tillett WS, Goebel WF, Avery OT. 119.  1930. Chemical and immunological properties of a species-specific carbohydrate of pneumococci. J. Exp. Med. 52:895–900 [Google Scholar]
  120. Tomasz A. 120.  1967. Choline in the cell wall of a bacterium: novel type of polymer-linked choline in Pneumococcus. Science 157:694–97 [Google Scholar]
  121. Tomasz A. 121.  1968. Biological consequences of the replacement of choline by ethanolamine in the cell wall of Pneumococcus: chain formation, loss of transformability, and loss of autolysis. Proc. Natl. Acad. Sci. USA 59:86–93 [Google Scholar]
  122. Tomasz A, Westphal M. 122.  1971. Abnormal autolytic enzyme in a pneumococcus with altered teichoic acid composition. Proc. Natl. Acad. Sci. USA 68:2627–30 [Google Scholar]
  123. Uchikawa K, Sekikawa I, Azuma I. 123.  1986. Structural studies on lipoteichoic acids from four Listeria strains. J. Bacteriol. 168:115–22 [Google Scholar]
  124. Volkman BF, Zhang Q, Debabov DV, Rivera E, Kresheck GC, Neuhaus FC. 124.  2001. Biosynthesis of d-alanyl-lipoteichoic acid: the tertiary structure of apo-d-alanyl carrier protein. Biochemistry 40:7964–72 [Google Scholar]
  125. Vollmer W, Tomasz A. 125.  2001. Identification of the teichoic acid phosphorylcholine esterase in Streptococcus pneumoniae. Mol. Microbiol. 39:1610–22 [Google Scholar]
  126. Voss S, Hallström T, Saleh M, Burchhardt G, Pribyl T. 126.  et al. 2013. The choline-binding protein PspC of Streptococcus pneumoniae interacts with the C-terminal heparin-binding domain of vitronectin. J. Biol. Chem. 288:15614–27 [Google Scholar]
  127. Weart RB, Lee AH, Chien AC, Haeusser DP, Hill NS, Levin PA. 127.  2007. A metabolic sensor governing cell size in bacteria. Cell 130:335–47 [Google Scholar]
  128. Webb AJ, Karatsa-Dodgson M, Gründling A. 128.  2009. Two-enzyme systems for glycolipid and polyglycerolphosphate lipoteichoic acid synthesis in Listeria monocytogenes. Mol. Microbiol. 74:299–314 [Google Scholar]
  129. Weisman LE, Thackray HM, Garcia-Prats JA, Nesin M, Schneider JH. 129.  et al. 2009. Phase 1/2 double-blind, placebo-controlled, dose escalation, safety, and pharmacokinetic study of pagibaximab (BSYX-A110), an antistaphylococcal monoclonal antibody for the prevention of staphylococcal bloodstream infections, in very-low-birth-weight neonates. Antimicrob. Agents Chemother. 53:2879–86 [Google Scholar]
  130. Weisman LE, Thackray HM, Steinhorn RH, Walsh WF, Lassiter HA. 130.  et al. 2011. A randomized study of a monoclonal antibody (pagibaximab) to prevent staphylococcal sepsis. Pediatrics 128:271–79 [Google Scholar]
  131. Wörmann ME, Corrigan RM, Simpson PJ, Matthews SJ, Gründling A. 131.  2011. Enzymatic activities and functional interdependencies of Bacillus subtilis lipoteichoic acid synthesis enzymes. Mol. Microbiol. 79:566–83 [Google Scholar]
  132. Wörmann ME, Reichmann NT, Malone CL, Horswill AR, Gründling A. 132.  2011. Proteolytic cleavage inactivates the Staphylococcus aureus lipoteichoic acid synthase. J. Bacteriol. 193:5279–91 [Google Scholar]
  133. Yokoyama K, Araki Y, Ito E. 133.  1988. The function of galactosyl phosphorylpolyprenol in biosynthesis of lipoteichoic acid in Bacillus coagulans. Eur. J. Biochem. 173:453–58 [Google Scholar]
  134. Yonus H, Neumann P, Zimmermann S, May JJ, Marahiel MA, Stubbs MT. 134.  2008. Crystal structure of DltA: implications for the reaction mechanism of non-ribosomal peptide synthetase adenylation domains. J. Biol. Chem. 283:32484–91 [Google Scholar]
  135. Zhang JR, Idanpaan-Heikkila I, Fischer W, Tuomanen EI. 135.  1999. Pneumococcal licD2 gene is involved in phosphorylcholine metabolism. Mol. Microbiol. 31:1477–88 [Google Scholar]
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