Wall teichoic acids of gram-positive bacteria

Annual Review of Microbiology

Volumn 67, Issue , 2013, Pages 313-336

  Brown, Stephanie ^a   Santa Maria Jr , John P ^a   Walker, Suzanne ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bacterial cell wall; Biofilm; d alanylation; MRSA; Peptidoglycan; Virulence factor

Indexed keywords

ANTIBIOTIC AGENT; BETA LACTAM; GLYCEROPHOSPHATE; PEPTIDOGLYCAN; POLY(GLYCEROL 3 PHOSPHATE); POLY(RIBITOL 5 PHOSPHATE); POLYMER; TEICHOIC ACID; UNCLASSIFIED DRUG; VIRULENCE FACTOR; WALL TEICHOIC ACID;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BIOSYNTHESIS; CELL SHAPE; CELL STRUCTURE; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; DRUG TARGETING; GRAM POSITIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; SYNTHESIS;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL WALL; GRAM-POSITIVE BACTERIA; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; TEICHOIC ACIDS;

EID: 84884512916     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092412-155620     Document Type: Article

References (151)

1. Allison SE, D?Elia MA, Arar S, Monteiro MA, Brown ED. 2011. Studies of the genetics, function, and kineticmechanism of TagE, the wall teichoic acid glycosyltransferase in Bacillus subtilis 168. J. Biol. Chem. 286:23708-16
2. Aly R, Shinefield HR, Litz C, Maibach HI. 1980. Role of teichoic acid in the binding of Staphylococcus aureus to nasal epithelial cells. J. Infect. Dis. 141:463-65
3. Anderson AJ, Green RS, Sturman AJ, Archibald AR. 1978. Cell wall assembly in Bacillus subtilis: location of wall material incorporated during pulsed release of phosphate limitation, its accessibility to bacteriophages and concanavalin A, and its susceptibility to turnover. J. Bacteriol. 136:886-99
4. Andre G, Deghorain M, Bron PA, van Swam II, Kleerebezem M, et al. 2011. Fluorescence and atomic force microscopy imaging of wall teichoic acids in Lactobacillus plantarum. ACS Chem. Biol. 6:366-76
5. Araki Y, Ito E. 1989. Linkage units in cell walls of gram-positive bacteria. Crit. Rev.Microbiol. 17:121-35
6. Armstrong JJ, Baddiley J, Buchanan JG, Carss B, Greenberg GR. 1958. Isolation and structure of ribitol phosphate derivatives (teichoic acids) from bacterial cell walls. J. Chem. Soc. 1958:4344-54
7. Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, et al. 2010. Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 107:18991-96
8. Baddiley J. 1970. Structure, biosynthesis, and function of teichoic acids. Acc. Chem. Res. 3:98-105
9. Badurina DS, Zolli-Juran M, Brown ED. 2003. CTP:glycerol 3-phosphate cytidylyltransferase (TarD) from Staphylococcus aureus catalyzes the cytidylyl transfer via an ordered Bi-Bi reaction mechanism with micromolar Km values. Biochim. Biophys. Acta 1646:196-206
10. Baptista C, Santos MA, S'ao-José C. 2008. Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J. Bacteriol. 190:4989-96
11. Baur S, Marles-Wright J, Buckenmaier S, Lewis RJ, Vollmer W. 2009. Synthesis of CDP-activated ribitol for teichoic acid precursors in Streptococcus pneumoniae. J. Bacteriol. 191:1200-10
12. Bera A, Biswas R, Herbert S, Kulauzovic E, Weidenmaier C, et al. 2007. Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J. Bacteriol. 189:280-83
13. Bernal P, Zloh M, Taylor PW. 2009. Disruption of D-alanyl esterification of Staphylococcus aureus cell wall teichoic acid by the β-lactam resistance modifier (-)-epicatechin gallate. J. Antimicrob. Chemother. 63:1156-62
14. Bhavsar AP, Beveridge TJ, Brown ED. 2001. Precise deletion of tagD and controlled depletion of its product, glycerol 3-phosphate cytidylyltransferase, leads to irregular morphology and lysis of Bacillus subtilis grown at physiological temperature. J. Bacteriol. 183:6688-93
15. Bhavsar AP, Erdman LK, Schertzer JW, Brown ED. 2004. Teichoic acid is an essential polymer in Bacillus subtilis that is functionally distinct from teichuronic acid. J. Bacteriol. 186:7865-73
16. Bhavsar AP, Truant R, Brown ED. 2005. The TagB protein in Bacillus subtilis 168 is an intracellular peripheral membrane protein that can incorporate glycerol phosphate onto amembrane-bound acceptor in vitro. J. Biol. Chem. 280:36691-700
17. Bierbaum G, Sahl HG. 1985. Induction of autolysis of staphylococci by the basic peptide antibiotics Pep 5 and nisin and their influence on the activity of autolytic enzymes. Arch. Microbiol. 141:249-54
18. Biswas R, Martinez RE, Gohring N, Schlag M, Josten M, et al. 2012. Proton-binding capacity of Staphylococcus aureus wall teichoic acid and its role in controlling autolysin activity. PLoS ONE 7:e41415
19. Boylan RJ, Mendelson NH, Brooks D, Young FE. 1972. Regulation of the bacterial cell wall: analysis of a mutant of Bacillus subtilis defective in biosynthesis of teichoic acid. J. Bacteriol. 110:281-90
20. Bracha R, Davidson R, Mirelman D. 1978. Defect in biosynthesis of the linkage unit between peptidoglycan and teichoic acid in a bacteriophage- resistant mutant of Staphylococcus aureus. J. Bacteriol. 134:412-17
21. Bron PA, Tomita S, van Swam II, Remus DM, MeijerinkM, et al. 2012. Lactobacillus plantarum possesses the capability for wall teichoic acid backbone alditol switching. Microb. Cell Fact. 11:123
22. Brown S, Meredith T, Swoboda J, Walker S. 2010. Staphylococcus aureus and Bacillus subtilis W23 make polyribitol wall teichoic acids using different enzymatic pathways. Chem. Biol. 17:1101-10
23. Brown S, Xia G, Luhachack LG, Campbell J, Meredith TC, et al. 2012. Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proc. Natl. Acad. Sci. USA 109:18909-14
24. Brown S, Zhang Y-H, Walker S. 2008. A revised pathway proposed for Staphylococcus aureus wall teichoic acid biosynthesis based on in vitro reconstitution of the intracellular steps. Chem. Biol. 15:12-21
25. Campbell J, Singh AK, Santa Maria JP Jr, Kim Y, Brown S, et al. 2011. Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus. ACS Chem. Biol. 6:106-16
26. Campbell J, Singh AK, Swoboda JG, Gilmore MS, Wilkinson BJ, Walker S. 2012. An antibiotic that inhibits a late step in wall teichoic acid biosynthesis induces the cell wall stress stimulon in Staphylococcus aureus. Antimicrob. Agents Chemother. 56:1810-20
27. Chatterjee AN, Mirelman D, SingerHJ, Park JT. 1969. Properties of a novel pleiotropic bacteriophageresistant mutant of Staphylococcus aureus H. J. Bacteriol. 100:846-53
28. ChildsWC III, Taron DJ, Neuhaus FC. 1985. Biosynthesis of D-alanyl-lipoteichoic acid by Lactobacillus casei: interchain transacylation of D-alanyl ester residues. J. Bacteriol. 162:1191-95
29. Chin T, Burger MM, Glaser L. 1966. Synthesis of teichoic acids. VI. The formation of multiple wall polymers in Bacillus subtilis W-23. Arch. Biochem. Biophys. 116:358-67
30. Clatworthy AE, Pierson E, Hung DT. 2007. Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol. 3:541-48
31. Cole RM, Popkin TJ, Boylan RJ, Mendelson NH. 1970. Ultrastructure of a temperature-sensitive rod? mutant of Bacillus subtilis. J. Bacteriol. 103:793-810
32. Collins LV, Kristian SA, Weidenmaier C, Faigle M, Van Kessel KPM, et al. 2002. Staphylococcus aureus strains lacking D-alaninemodifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J. Infect. Dis. 186:214-19
33. Davison AL, Baddiley J. 1964. Teichoic acids in the walls of Staphylococci: glycerol teichoic acids in walls of Staphylococcus epidermidis. Nature 202:874
34. Debabov DV, Kiriukhin MY, Neuhaus FC. 2000. Biosynthesis of lipoteichoic acid in Lactobacillus rhamnosus: role of DltD in D-alanylation. J. Bacteriol. 182:2855-64
35. D'elia MA, Henderson JA, Beveridge TJ, Heinrichs DE, Brown ED. 2009. The N-acetylmannosamine transferase catalyzes the first committed step of teichoic acid assembly in Bacillus subtilis and Staphylococcus aureus. J. Bacteriol. 191:4030-34
36. Delia MA, Millar KE, Beveridge TJ, Brown ED. 2006. Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J. Bacteriol. 188:8313-16
37. Delia MA, Millar KE, Bhavsar AP, Tomljenovic AM, Hutter B, et al. 2009. Probing teichoic acid genetics with bioactive molecules reveals new interactions among diverse processes in bacterial cell wall biogenesis. Chem. Biol. 16:548-56
38. Delia MA, Pereira MP, Chung YS, Zhao W, Chau A, et al. 2006. Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J. Bacteriol. 188:4183-89
39. DenapaiteD, Bruckner R, Hakenbeck R, Vollmer W. 2012. Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species: lessons from genomes. Microb. Drug Resist. 18:344-58
40. Dengler V, Meier PS, Heusser R, Kupferschmied P, Fazekas J, et al. 2012. Deletion of hypothetical wall teichoic acid ligases in Staphylococcus aureus activates the cell wall stress response. FEMS Microbiol. Lett. 333:109-20
41. Dreisbach A, van Dijl JM, Buist G. 2011. The cell surface proteome of Staphylococcus aureus. Proteomics 11:3154-68
42. Eberhardt A, Hoyland CN, Vollmer D, Bisle S, Cleverley RM, et al. 2012. Attachment of capsular polysaccharide to the cell wall in Streptococcus pneumoniae. Microb. Drug Resist. 18:240-55
43. Elbaz M, Ben-Yehuda S. 2010. The metabolic enzyme ManA reveals a link between cell wall integrity and chromosome morphology. PLoS Genet. 6:e1001119
44. Ellwood DC. 1970. The wall content and composition of Bacillus subtilis var. niger grown in a chemostat. Biochem. J. 118:367-73
45. Endl J, SeidlHP, Fiedler F, Schleifer KH. 1983. Chemical composition and structure of cell wall teichoic acids of staphylococci. Arch. Microbiol. 135:215-23
46. Endl J, Seidl PH, Fiedler F, Schleifer KH. 1984. Determination of cell wall teichoic acid structure of staphylococci by rapid chemical and serological screening methods. Arch. Microbiol. 137:272-80
47. Eugster MR, Loessner MJ. 2012. Wall teichoic acids restrict access of bacteriophage endolysin Ply118, Ply511, and PlyP40 cell wall binding domains to the Listeria monocytogenes peptidoglycan. J. Bacteriol. 194:6498-506
48. FarhaMA, Leung A, Sewell EW, Delia MA, Allison SE, et al. 2013. Inhibition ofWTAsynthesis blocks the cooperative action of PBPs and sensitizes MRSA to β-lactams. ACS Chem. Biol. 8:226-33
49. Fischer W, Rosel P, Koch HU. 1981. Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcus aureus. J. Bacteriol. 146:467-75
50. Fitzgerald SN, Foster TJ. 2000. Molecular analysis of the tagF gene, encoding CDPglycerol: poly(glycerophosphate) glycerophosphotransferase of Staphylococcus epidermidis ATCC 14990. J. Bacteriol. 182:1046-52
51. Formstone A, Carballido-López R, Noirot P, Errington J, Scheffers D-J. 2008. Localization and interactions of teichoic acid synthetic enzymes in Bacillus subtilis. J. Bacteriol. 190:1812-21
52. Frankel MB, Schneewind O. 2012. Determinants of murein hydrolase targeting to cross-wall of Staphylococcus aureus peptidoglycan. J. Biol. Chem. 287:10460-71
53. Geddes AM, Klugman KP, Rolinson GN. 2007. Introduction: historical perspective and development of amoxicillin/clavulanate. Int. J. Antimicrob. Agents 30(Suppl. 2):S109-12
54. Ginsberg C, Zhang Y-H, Yuan Y, Walker S. 2006. In vitro reconstitution of two essential steps in wall teichoic acid biosynthesis. ACS Chem. Biol. 1:25-28
55. Gross M, Cramton SE, Götz F, Peschel A. 2001. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun. 69:3423-26
56. Haas R, Koch HU, Fischer W. 1984. Alanyl turnover from lipoteichoic acid to teichoic acid in Staphylococcus aureus. FEMS Microbiol. Lett. 21:27-31
57. Hancock I, Wiseman G, Baddiley J. 1976. Biosynthesis of the unit that links teichoic acid to the bacterial wall: inhibition by tunicamycin. FEBS Lett. 69:75-80
58. Heaton MP, Neuhaus FC. 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
59. Heaton MP, Neuhaus FC. 1994. Role of the D-alanyl carrier protein in the biosynthesis of D-alanyllipoteichoic acid. J. Bacteriol. 176:681-90
60. Heptinstall S, Archibald AR, Baddiley J. 1970. Teichoic acids and membrane function in bacteria. Nature 225:519-21
61. Holland L, Conlon B, O'Gara JP. 2010. Mutation of tagO reveals an essential role for wall teichoic acids in Staphylococcus epidermidis biofilm development. Microbiology 157:408-18
62. Hubscher J, McCallum N, Sifri CD, Majcherczyk PA, Entenza JM, et al. 2009. MsrR contributes to cell surface characteristics and virulence in Staphylococcus aureus. FEMS Microbiol. Lett. 295:251-60
63. JamesDB, Yother J. 2012. Genetic and biochemical characterizations of enzymes involved in Streptococcus pneumoniae serotype 2 capsule synthesis demonstrate that Cps2T (WchF) catalyzes the committed step by addition of β1-4 rhamnose, the second sugar residue in the repeat unit. J. Bacteriol. 194:6479-89
64. Jenni R, Berger-Bächi B. 1998. Teichoic acid content in different lineages of Staphylococcus aureus NCTC8325. Arch. Microbiol. 170:171-78
65. Karamata D, Pooley HM, Monod M. 1987. Expression of heterologous genes for wall teichoic acid in Bacillus subtilis 168. Mol. Gen. Genet. 207:73-81
66. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S, et al. 2011. A widespread family of bacterial cell wall assembly proteins. EMBO J. 30:4931-41
67. Kern T, Giffard M, Hediger S, Amoroso A, Giustini C, et al. 2010. Dynamics characterization of fully hydrated bacterial cell walls by solid-state NMR: evidence for cooperative binding of metal ions. J. Am. Chem. Soc. 132:10911-19
68. KiriukhinMY, Neuhaus FC. 2001. D-alanylation of lipoteichoic acid: role of the D-alanyl carrier protein in acylation. J. Bacteriol. 183:2051-58
69. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, et al. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100:4678-83
70. Kohler T, Weidenmaier C, Peschel A. 2009. Wall teichoic acid protects Staphylococcus aureus against antimicrobial fatty acids from human skin. J. Bacteriol. 191:4482-84
71. Kojima N, Araki Y, Ito E. 1985. Structure of the linkage units between ribitol teichoic acids and peptidoglycan. J. Bacteriol. 161:299-306
72. Kovács M, Halfmann A, Fedtke I, Heintz M, Peschel A, 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
73. Kristian SA, Datta V, Weidenmaier C, Kansal R, Fedtke I, 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
74. Kristian SA, Lauth X, Nizet V, Goetz F, Neumeister B, et al. 2003. Alanylation of teichoic acids protects Staphylococcus aureus against Toll-like receptor 2-dependent host defense in a mouse tissue cage infection model. J. Infect. Dis. 188:414-23
75. Lazarevic V, Abellan F-X, Möller SB, Karamata D, Mauël C. 2002. Comparison of ribitol and glycerol teichoic acid genes in Bacillus subtilis W23 and 168: identical function, similar divergent organization, but different regulation. Microbiology 148:815-24
76. Lazarevic V, Karamata D. 1995. The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two wall teichoic acids. Mol. Microbiol. 16:345-55
77. Lee K, Campbell J, Swoboda JG, Cuny GD, Walker S. 2010. Development of improved inhibitors of wall teichoic acid biosynthesis with potent activity against Staphylococcus aureus. Bioorgan. Med. Chem. Lett. 20:1767-70
78. Lovering AL, Lin LY-C, Sewell EW, Spreter T, Brown ED, Strynadka NCJ. 2010. Structure of the bacterial teichoic acid polymerase TagF provides insights into membrane association and catalysis. Nat. Struct. Mol. Biol. 17:582-89
79. Maki H, Yamaguchi T, Murakami K. 1994. Cloning and characterization of a gene affecting the methicillin resistance level and the autolysis rate in Staphylococcus aureus. J. Bacteriol. 176:4993-5000
80. Matias VR, Beveridge TJ. 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
81. Matias VR, Beveridge TJ. 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
82. Matias VR, Beveridge TJ. 2007. Cryo-electronmicroscopy of cell division in Staphylococcus aureus reveals a mid-zone between nascent cross walls. Mol. Microbiol. 64:195-206
83. Mauck J, Glaser L. 1972. On the mode of in vivo assembly of the cell wall of Bacillus subtilis. J. Biol. Chem. 247:1180-87
84. May JJ, Finking R, Wiegeshoff F, Weber TT, Bandur N, 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
85. Meredith TC, Swoboda JG, Walker S. 2008. Late-stage polyribitol phosphate wall teichoic acid biosynthesis in Staphylococcus aureus. J. Bacteriol. 190:3046-56
86. Mericl AN, Friesen JA. 2012. Comparative kinetic analysis of glycerol 3-phosphate cytidylyltransferase from Enterococcus faecalis and Listeria monocytogenes. Med. Sci. Monit. 18:427-34
87. Minnig K, Lazarevic V, Soldo B, Mauël C. 2005. Analysis of teichoic acid biosynthesis regulation reveals that the extracytoplasmic function sigma factor M is induced by phosphate depletion in Bacillus subtilis W23. Microbiology 151:3041-49
88. Nathenson SG, Ishimoto N, Anderson JS, Strominger JL. 1966. Enzymatic synthesis and immunochemistry of α- and β-N-acetylglucosaminylribitol linkages in teichoic acids from several strains of Staphylococcus aureus. J. Biol. Chem. 241:651-58
89. Naumova IB, Kuznetsov VD, Kudrina KS, Bezzubenkova AP. 1980. The occurrence of teichoic acids in streptomycetes. Arch. Microbiol. 126:71-75
90. Naumova IB, Shashkov AS, Tul'skaya EM, StreshinskayaGM, Kozlova YI, et al. 2001. Cell wall teichoic acids: structural diversity, species specificity in the genus Nocardiopsis, and chemotaxonomic perspective. FEMS Microbiol. Rev. 25:269-84
91. Neuhaus FC, Baddiley J. 2003. A continuum of anionic charge: structures and functions of D-alanylteichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67:686-723
92. Over B, Heusser R, McCallum N, Schulthess B, Kupferschmied P, et al. 2011. LytR-CpsA-Psr proteins in Staphylococcus aureus display partial functional redundancy and the deletion of all three severely impairs septum placement and cell separation. FEMS Microbiol. Lett. 320:142-51
93. Park JT, Shaw DR, Chatterjee AN, Mirelman D, Wu T. 1974. Mutants of staphylococci with altered cell walls. Ann. N. Y. Acad. Sci. 236:54-62
94. Park YS, Sweitzer TD, Dixon JE, Kent C. 1993. Expression, purification, and characterization of CTP:glycerol-3-phosphate cytidylyltransferase from Bacillus subtilis. J. Biol. Chem. 268:16648-54
95. Perego M, Glaser P, Minutello A, StrauchMA, Leopold K, Fischer W. 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
96. Pereira MP, Brown ED. 2004. Bifunctional catalysis by CDP-ribitol synthase: convergent recruitment of reductase and cytidylyltransferase activities in Haemophilus influenzae and Staphylococcus aureus. Biochemistry 43:11802-12
97. PereiraMP, Delia MA, Troczynska J, Brown ED. 2008. Duplication of teichoic acid biosynthetic genes in Staphylococcus aureus leads to functionally redundant poly(ribitol phosphate) polymerases. J. Bacteriol. 190:5642-49
98. Pereira MP, Schertzer JW, Delia MA, Koteva KP, Hughes DW, et al. 2008. The wall teichoic acid polymerase TagF efficiently synthesizes poly(glycerol phosphate) on the TagB product lipid III. ChemBioChem 9:1385-90
99. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Götz F. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405-10
100. Peschel A, Vuong C, Otto M, Götz F. 2000. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob. Agents Chemother. 44:2845-47
101. Pooley HM, Karamata D. 2000. Incorporation of [2-3H]glycerol into cell surface components of Bacillus subtilis 168 and thermosensitive mutants affected in wall teichoic acid synthesis: effect of tunicamycin. Microbiology 146:797-805
102. Potekhina NV, Streshinskaya GM, Tul'skaya EM, Kozlova YI, Senchenkova SN, Shashkov AS. 2011. Phosphate-containing cell wall polymers of bacilli. Biochemistry (Moscow) 76:745-54
103. Price N, Tsvetanova B. 2007. Biosynthesis of the tunicamycins: a review. J. Antibiot. 60:485-91
104. Qamar A, Golemi-Kotra D. 2012. Dual roles of FmtA in Staphylococcus aureus cell wall biosynthesis and autolysis. Antimicrob. Agents Chemother. 56:3797-805
105. Qian Z, Yin Y, Zhang Y, Lu L, Li Y, Jiang Y. 2006. Genomic characterization of ribitol teichoic acid synthesis in Staphylococcus aureus: genes, genomic organization and gene duplication. BMC Genomics 7:74
106. Reichmann NT, Gr ündling A. 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
107. Rubinchik E, Schneider T, Elliott M, Scott WR, Pan J, et al. 2011. Mechanism of action and limited cross-resistance of new lipopeptide MX-2401. Antimicrob. Agents Chemother. 55:2743-54
108. Saar-Dover R, Bitler A, Nezer R, Shmuel-Galia L, Firon A, 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
109. Schertzer JW, Brown ED. 2003. Purified, recombinant TagF protein from Bacillus subtilis 168 catalyzes the polymerization of glycerol phosphate onto a membrane acceptor in vitro. J. Biol. Chem. 278:18002-7
110. Schertzer JW, Brown ED. 2008. Use of CDP-glycerol as an alternate acceptor for the teichoic acid polymerase reveals that membrane association regulates polymer length. J. Bacteriol. 190:6940-47
111. Schirner K, Stone LK, Walker S. 2011. ABC transporters required for export of wall teichoic acids do not discriminate between different main chain polymers. ACS Chem. Biol. 6:407-12
112. SchlagM, Biswas R, Krismer B, Kohler T, Zoll S, et al. 2010. Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol. Microbiol. 75:864-73
113. Sewell EWC, PereiraMP, Brown ED. 2009. The wall teichoic acid polymerase TagF is non-processive in vitro and amenable to study using steady state kinetic analysis. J. Biol. Chem. 284:21132-38
114. Silhavy TJ, Kahne D, Walker S. 2010. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2:a000414
115. Smith T, Blackman S, Foster S. 2000. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249-62
116. Soldo B, LazarevicV, KaramataD. 2002. tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148:2079-87
117. Soldo B, Lazarevic V, Pooley HM, Karamata D. 2002. Characterization of a Bacillus subtilis thermosensitive teichoic acid-deficient mutant: gene mnaA ( yvyH) encodes the UDP-N-acetylglucosamine 2-epimerase. J. Bacteriol. 184:4316-20
118. Suzuki T, Campbell J, Swoboda JG, Walker S, GilmoreMS. 2011. Role of wall teichoic acids in Staphylococcus aureus endophthalmitis. Investig. Ophthalmol. Vis. Sci. 52:3187-92
119. Suzuki T, Swoboda JG, Campbell J, Walker S, GilmoreMS. 2011. In vitro antimicrobial activity of wall teichoic acid biosynthesis inhibitors against Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 55:767-74
120. Swoboda JG, Campbell J, Meredith TC, Walker S. 2010. Wall teichoic acid function, biosynthesis, and inhibition. ChemBioChem 11:35-45
121. Swoboda JG, Meredith TC, Campbell J, Brown S, Suzuki T, et al. 2009. Discovery of a small molecule that blocks wall teichoic acid biosynthesis in Staphylococcus aureus. ACS Chem. Biol. 4:875-83
122. Theilacker C, Holst O, Lindner B, Huebner J, Kaczynski Z. 2012. The structure of the wall teichoic acid isolated from Enterococcus faecalis strain 12030. Carbohydr. Res. 354:106-9
123. Tomasz A, McDonnell M, Westphal M, Zanati E. 1975. Coordinated incorporation of nascent peptidoglycan and teichoic acid into pneumococcal cell walls and conservation of peptidoglycan during growth. J. Biol. Chem. 250:337-41
124. Tomita S, Irisawa T, Tanaka N, Nukada T, Satoh E, et al. 2010. Comparison of components and synthesis genes of cell wall teichoic acid among Lactobacillus plantarum strains. Biosci. Biotechnol. Biochem. 74:928-33
125. ToriiM, Kabat EA, Bezer AE. 1964. Separation of teichoic acid of Staphylococcus aureus into two immunologically distinct specific polysaccharides with α- and β-N-acetylglucosaminyl linkages respectively: antigenicity of teichoic acids in man. J. Exp. Med. 120:13-29
126. Vadyvaloo V, Arous S, Gravesen A, Héchard Y, Chauhan-Haubrock R, et al. 2004. Cell-surface alterations in class IIa bacteriocin-resistant Listeria monocytogenes strains. Microbiology 150:3025-33
127. Vergara-Irigaray M, Maira-Litrán T, Merino N, Pier GB, Penadés JR, Lasa I. 2008. Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology 154:865-77
128. Vinogradov E, Sadovskaya I, Li J, Jabbouri S. 2006. Structural elucidation of the extracellular and cellwall teichoic acids of Staphylococcus aureus MN8m, a biofilm forming strain. Carbohydr. Res. 341:738-43
129. Volkman BF, Zhang Q, Debabov DV, Rivera E, Kresheck GC, Neuhaus FC. 2001. Biosynthesis of D-alanyl-lipoteichoic acid: the tertiary structure of apo-D-alanyl carrier protein. Biochemistry 40:7964-72
130. Vollmer W, Blanot D, de Pedro MA. 2008. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32:149-67
131. Walter J, Loach DM, Alqumber M, Rockel C, Hermann C, et al. 2007. D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ. Microbiol. 9:1750-60
132. Wang H, Gill CJ, Lee SH, Mann P, Zuck P, et al. 2013. Discovery of wall teichoic acid inhibitors as potential anti-MRSA β-lactam combination agents. Chem. Biol. 20:272-84
133. Ward JB. 1981. Teichoic and teichuronic acids: biosynthesis, assembly, and location. Microbiol. Rev. 45:211-43
134. Wecke J, Madela K, Fischer W. 1997. The absence of D-alanine from lipoteichoic acid and wall teichoic acid alters surface charge, enhances autolysis and increases susceptibility to methicillin in Bacillus subtilis. Microbiology 143:2952-60
135. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, et al. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10:243-45
136. Weidenmaier C, Kokai-Kun JF, Kulauzovic E, Kohler T, Thumm G, et al. 2008. Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int. J. Med. Microbiol. 298:505-13
137. Weidenmaier C, Kristian SA, Peschel A. 2003. Bacterial resistance to antimicrobial host defenses-an emerging target for novel antiinfective strategies? Curr. Drug Targets 4:643-49
138. Weidenmaier C, Peschel A. 2008. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6:276-87
139. Weidenmaier C, Peschel A, Xiong Y-Q, Kristian SA, Dietz K, et al. 2005. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J. Infect. Dis. 191:1771-77
140. Wickham JR, Halye JL, Kashtanov S, Khandogin J, Rice CV. 2009. Revisiting magnesium chelation by teichoic acid with phosphorus solid-state NMR and theoretical calculations. J. Phys. Chem. B 113:2177-83
141. Wyke AW, Ward JB. 1977. Biosynthesis of wall polymers in Bacillus subtilis. J. Bacteriol. 130:1055-63
142. Xayarath B, Yother J. 2007. Mutations blocking side chain assembly, polymerization, or transport of a Wzy-dependent Streptococcus pneumoniae capsule are lethal in the absence of suppressor mutations and can affect polymer transfer to the cell wall. J. Bacteriol. 189:3369-81
143. XiaG, Corrigan RM, WinstelV, GoerkeC, Gr ündling A, Peschel A. 2011. Wall teichoic acid-dependent adsorption of staphylococcal siphovirus and myovirus. J. Bacteriol. 193:4006-9
144. Xia G, Kohler T, Peschel A. 2010. The wall teichoic acid and lipoteichoic acid polymers of Staphylococcus aureus. Int. J. Med. Microbiol. 300:148-54
145. Xia G, Maier L, Sanchez-Carballo P, Li M, Otto M, et al. 2010. Glycosylation of wall teichoic acid in Staphylococcus aureus by TarM. J. Biol. Chem. 285:13405-15
146. Yamamoto H, Miyake Y, Hisaoka M, Kurosawa S-I, Sekiguchi J. 2008. The major and minor wall teichoic acids prevent the sidewall localization of vegetative DL-endopeptidase LytF in Bacillus subtilis. Mol. Microbiol. 70:297-310
147. Yokoyama K, Miyashita T, Araki Y, Ito E. 1986. Structure and functions of linkage unit intermediates in the biosynthesis of ribitol teichoic acids in Staphylococcus aureus H and Bacillus subtilis W23. Eur. J. Biochem. 161:479-89
148. YoungM, Mauël C, Margot P, Karamata D. 1989. Pseudo-allelic relationship between non-homologous genes concerned with biosynthesis of polyglycerol phosphate and polyribitol phosphate teichoic acids in Bacillus subtilis strains 168 andW23. Mol. Microbiol. 3:1805-12
149. Zapun A, Contreras-Martel C, Vernet T. 2008. Penicillin-binding proteins and β-lactam resistance. FEMS Microbiol. Rev. 32:361-85
150. Zhang Y-H, Ginsberg C, Yuan Y, Walker S. 2006. Acceptor substrate selectivity and kinetic mechanism of Bacillus subtilis TagA. Biochemistry 45:10895-904
151. Zolli M, Kobric D, Brown E. 2001. Reduction precedes cytidylyl transfer without substrate channeling in distinct active sites of the bifunctional CDP-ribitol synthase from Haemophilus influenzae. Biochemistry 40:5041-48