FemABX peptidyl transferases: A link between branched-chain cell wall peptide formation and β-lactam resistance in gram-positive cocci

Antimicrobial Agents and Chemotherapy

Volumn 47, Issue 3, 2003, Pages 837-846

  Rohrer, S ^a   Berger Bachi B ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN; PEPTIDYLTRANSFERASE; PROTEIN FEMABX; UNCLASSIFIED DRUG; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIOLYSIS; BINDING AFFINITY; DRUG INACTIVATION; DRUG MECHANISM; DRUG TARGETING; ENTEROCOCCUS; GENE MUTATION; GRAM POSITIVE COCCI; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; SHORT SURVEY; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMS; CARRIER PROTEINS; CELL DIVISION; CELL WALL; GRAM-POSITIVE COCCI; HEXOSYLTRANSFERASES; HUMANS; MEMBRANE PROTEINS; MURAMOYLPENTAPEPTIDE CARBOXYPEPTIDASE; PENICILLIN-BINDING PROTEINS; PEPTIDE BIOSYNTHESIS; PEPTIDYL TRANSFERASES; VANCOMYCIN RESISTANCE;

EID: 0037416970     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.47.3.837-846.2003     Document Type: Short Survey

References (117)

1. Alborn, W. E. J., J. Hoskins, S. Unal, J. E. Flokowitsch, C. A. Hayes, J. E. Dotzlaf, W. K. Yeh, and P. L. Skatrud. 1996. Cloning and characterization of femA and femB from Staphylococcus epidermidis. Gene 180:177-181.
2. al-Obeid, S., D. Billot-Klein, J. van Heijenoort, E. Collatz, and L. Gutmann. 1992. Replacement of the essential penicillin-binding protein 5 by high-molecular mass PBPs may explain vancomycin-beta-lactam synergy in low-level vancomycin-resistant Enterococcus faecium D366. FEMS Microbiol. Lett. 70:79-84.
3. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Baba, T., F. Takeuchi, M. Kuroda, H. Yuzawa, K. Aoki, A. Oguchi, Y. Nagai, N. Iwama, K. Asano, T. Naimi, H. Kuroda, L. Cui, K. Yamamoto, and K. Hiramatsu. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819-1827.
5. Barber, M. 1961. Methicillin-resistant staphylococci. J. Clin. Pathol. 14:385-393.
6. Barg, N., H. Chambers, and D. Kernodle. 1991. Borderline susceptibility to antistaphylococcal penicillins is not conferred exclusively by the overproduction of beta-lactamase. Antimicrob. Agents Chemother. 35:1975-1979.
7. Beatson, S., G. Sloan, and R. Simmonds. 1998. Zoocin A immunity factor: a femA-like gene found in a group C streptococcus. FEMS Microbiol. Lett. 163:73-77.
8. Berger-Bächi, B. 1989. Genetics of methicillin resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 23:671-673.
9. Berger-Bächi, B. 1983. Insertional inactivation of staphylococcal methicillin resistance by Tn551. J. Bacteriol. 154:479-487.
10. Berger-Bächi, B., L. Barberis-Maino, A. Strässle, and F. H. Kayser. 1989. FemA, a host-mediated factor essential for methicillin resistance in Staphylococcus aureus: molecular cloning and characterization. Mol. Gen. Genet. 219:263-269.
11. Berger-Bächi, B., and S. Rohrer. 2002. Control of methicillin resistance in Staphylococcus aureus. Arch. Microbiol. 178:165-171.
12. Berger-Bächi, B., A. Strässle, J. E. Gustafson, and F. H. Kayser. 1992. Mapping and characterization of multiple chromosomal factors involved in methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 36:1367-1373.
13. Beukes, M., and J. W. Hastings. 2001. Self-protection against cell wall hydrolysis in Streptococcus milleri NMSCC 061 and analysis of the millericin B operon. Appl. Environ. Microbiol. 67:3888-3896.
14. Bierne, H., S. K. Mazmanian, M. Trost, M. G. Pucciarelli, G. Liu, P. Dehoux, L. Jansch, F. G. Portillo, O. Schneewind, and P. Cossart. 2002. Inactivation of the srtA gene in Listeria monocytogenes inhibits anchoring of surface proteins and affects virulence. Mol. Microbiol. 43:869-881.
15. Billot-Klein, D., D. Shlaes, D. Bryant, D. Bell, J. van Heijenoort, and L. Gutmann. 1996. Peptidoglycan structure of Enterococcus faecium expressing vancomycin resistance of the VanB type. Biochem. J. 313:711-715.
16. Bouhss, A., N. Josseaume, D. Allanic, M. Crouvoisier, L. Gutmann, J.-L. Mainardi, D. Mengin-Lecreulx, J. van Heijenoort, and M. Arthur. 2001. Identification of the UDP-MurNAc-pentapeptide:L-alanine ligase for synthesis of branched peptidoglycan precursors in Enterococcus faecalis. J. Bacteriol. 183:5122-5127.
17. Bugg, T. 1999. Bacterial peptidoglycan biosynthesis and its inhibition, p. 241-294. In M. Pinto (ed.), Comprehensive natural products chemistry, vol. 3. Elsevier, Oxford, United Kingdom.
18. Bumsted, R. M., J. L. Dahl, D. Soll, and J. L. Strominger. 1968. Biosynthesis of the peptidoglycan of bacterial cell walls. X. Further study of the glycyl transfer ribonucleic acids active in peptidoglycan synthesis in Staphylococcus aureus. J. Biol. Chem. 243:779-782.
19. Centers for Disease Control and Prevention. 2002. Staphylococcus aureus resistant to vancomycin - United States, 2002. Morb. Mortal. Wkly. Rep. 51:565-567.
20. DeHart, H. P., H. E. Heath, L. S. Heath, P. A. LeBlanc, and G. L. Sloan. 1995. The lysostaphin endopeptidase resistance gene (epr) specifies modification of peptidoglycan cross bridges in Staphylococcus simulans and Staphylococcus aureus. Appl. Environ. Microbiol. 61:1475-1479.
21. de Jonge, B. L., S. Handwerger, and D. Gage. 1996. Altered peptidoglycan composition in vancomycin-resistant Enterococcus faecalis. Antimicrob. Agents Chemother. 40:863-869.
22. de Jonge, B. L. M., Y. S. Chang, N. Xu, and D. Gage. 1996. Effect of exogenous glycine on peptidoglycan composition and resistance in a methicillin-resistant Staphylococcus aureus strain. Antimicrob. Agents Chemother. 40:1498-1503.
23. de Jonge, B. L. M., D. Gage, and N. Xu. 2002. The carboxyl terminus of peptidoglycan stem peptides is a determinant for methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 46:3151-3155.
24. de Jonge, B. L. M., T. Sidow, Y. S. Chang, H. Labischinski, B. Berger-Bächi, D. A. Gage, and A. Tomasz. 1993. Altered muropeptide composition in Staphylococcus aureus strains with an inactivated femA locus. J. Bacteriol. 175:2779-2782.
25. de Jonge, B. L. M., and A. Tomasz. 1993. Abnormal peptidoglycan produced in a methicillin-resistant strain of Staphylococcus aureus grown in the presence of methicillin: functional role for penicillin-binding protein 2A in cell wall synthesis. Antimicrob. Agents Chemother. 37:342-346.
26. de Lencastre, H., and A. Tomasz. 1994. Reassessment of the number of auxiliary genes essential for expression of high-level methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 38:2590-2598.
27. Dessen, A., N. Mouz, E. Gordon, J. Hopkins, and O. Dideberg. 2001. Crystal structure of PBP2x from a highly penicillin-resistant Streptococcus pneumoniae clinical isolate. J. Biol. Chem. 276:45106-45112.
28. Ehlert, K., W. Schröder, and H. Labischinski. 1997. Specificities of FemA and FemB for different glycine residues: FemB cannot substitute for FemA in staphylococcal peptidoglycan pentaglycine side chain formation. J. Bacteriol. 179:7573-7576.
29. Ehlert, K., M. Tschierske, C. Mori, W. Schröder, and B. Berger-Bächi. 2000. Site-specific serine incorporation by Lif and Epr into positions 3 and 5 of the staphylococcal peptidoglycan interpeptide bridge. J. Bacteriol. 182:2635-2638.
30. Filipe, S. R., E. Severina, and A. Tomasz. 2000. Distribution of the mosaic structured murM genes among natural populations of Streptococcus pneumoniae. J. Bacteriol. 182:6798-6805.
31. Filipe, S. R., E. Severina, and A. Tomasz. 2001. Functional analysis of Streptococcus pneumoniae MurM reveals the region responsible for its specificity in the synthesis of branched cell wall peptides. J. Biol. Chem. 276:39618.
32. Filipe, S. R., E. Severina, and A. Tomasz. 2001. The role of murMN operon in penicillin resistance and antibiotic tolerance of Streptococcus pneumoniae. Microb. Drug Resist. 7:303-316.
33. Filipe, S. R., and A. Tomasz. 2000. Inhibition of the expression of penicillin resistance in Streptococcus pneumoniae by inactivation of cell wall muropeptide branching genes. Proc. Natl. Acad. Sci. USA 97:4891-4896.
34. Fontana, R., M. Aldegheri, M. Ligozzi, H. Lopez, A. Sucari, and G. Satta. 1994. Overproduction of a low-affinity penicillin-binding protein and highlevel ampicillin resistance in Enterococcus faecium. Antimicrob. Agents Chemother. 38:1980-1983.
35. Fontana, R., P. Canepari, M. M. Lleo, and G. Satta. 1990. Mechanisms of resistance of enterococci to beta-lactam antibiotics. Eur. J. Clin. Microbiol. Infect. Dis. 9:103-105.
36. Garcia-Bustos, J., and A. Tomasz. 1990. A biological price of antibiotic resistance: major changes in the peptidoglycan structure of penicillin-resistant pneumococci. Proc. Natl. Acad. Sci. USA 87:5415-5419.
37. Ghuysen, J.-M. 1997. Penicillin-binding proteins. Wall peptidoglycan assembly and resistance to penicillin: facts, doubts and hopes. Int. J. Antimicrob. Agents 8:45-60.
38. Giesbrecht, P., T. Kersten, H. Maidhof, and J. Wecke. 1998. Staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin. Microbiol. Mol. Biol. Rev. 62:1371-1414.
39. Goffin, C., and J. M. Ghuysen. 1998. Multimodular penicillin binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079-1093.
40. Gordon, E., N. Mouz, E. Duée, and O. Dideberg. 2000. The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance. J. Mol. Biol. 299:477-485.
41. Grebe, T., and R. Hakenbeck. 1996. Penicillin-binding proteins 2b and 2x of Streptococcus pneumoniae are primary resistance determinants for different classes of beta-lactam antibiotics. Antimicrob. Agents Chemother. 40:829-834.
42. Gutmann, L., S. al-Obeid, D. Billot-Klein, M. L. Guerrier, and E. Collatz. 1994. Synergy and resistance to synergy between beta-lactam antibiotics and glycopeptides against glycopeptide-resistant strains of Enterococcus faecium. Antimicrob. Agents Chemother. 38:824-829.
43. Hackbarth, C. J., and H. F. Chambers. 1989. Methicillin-resistant staphylococci: genetics and mechanisms of resistance. Antimicrob. Agents Chemother. 33:991-994.
44. Hakenbeck, R., N. Balmelle, B. Weber, C. Gardes, W. Keck, and A. de Saizieu. 2001. Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae. Infect. Immun. 69:2477-2486.
45. Hakenbeck, R., and J. Coyette. 1998. Resistant penicillin-binding proteins. Cell. Mol. Life Sci. 54:332-340.
46. Hakenbeck, R., T. Grebe, D. Zahner, and J. B. Stock. 1999. Beta-lactam resistance in Streptococcus pneumoniae: penicillin-binding proteins and non-penicillin-binding proteins. Mol. Microbiol. 33:673-678.
47. r penicillin-binding protein variants during transfer of high-level beta-lactam resistance from Streptococcus mitis to Streptococcus pneumoniae. J. Bacteriol. 180:1831-1840.
48. Hegde, S. S., and T. E. Shrader. 2001. FemABX family members are novel nonribosomal peptidyltransferases and important pathogen-specific drug targets. J. Biol. Chem. 276:6998-7003.
49. Henze, U., T. Sidow, J. Wecke, H. Labischinski, and B. Berger-Bächi. 1993. Influence of femB on methicillin resistance and peptidoglycan metabolism in Staphylococcus aureus. J. Bacteriol. 175:1612-1620.
50. Henze, U. U., M. Roos, and B. Berger-Bächi. 1996. Effects of penicillin-binding protein 4 overproduction in Staphylococcus aureus. Microb. Drug Resist. Mech. Epidemiol. Dis. 2:193-199.
51. Hiramatsu, K., L. Cui, M. Kuroda, and T. Ito. 2001. The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol. 9:486-493.
52. Holt, J. 1994. Bergey's manual of determinative bacteriology, 9th ed. The Williams & Wilkins Co., Baltimore, Md.
53. Höltje, J. V. 1996. A hypothetical holoenzyme involved in the replication of the murein sacculus of Escherichia coli. Microbiology (United Kingdom) 142:1911-1918.
54. Ito, T., Y. Katayama, and K. Hiramatsu. 1999. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob. Agents Chemother. 43:1449-1458.
55. Jamin, M., R. Hakenbeck, and J. M. Frère. 1993. Penicillin binding protein 2x as a major contributor to intrinsic beta-lactam resistance of Streplococcus pneumoniae. FEBS Lett. 331:101-104.
56. Kamiryo, T., and M. Matsuhashi. 1972. The biosynthesis of the crosslinking peptides in the cell wall peptidoglycan of Staphylococcus aureus. J. Biol. Chem. 247:6306-6311.
57. Kamiryo, T., and M. Matsuhashi. 1969. Sequential addition of glycine from glycyl-tRNA to the lipid-linked precursors of cell wall peptidoglycan in Staphylococcus aureus. Biochem. Biophys. Res. Commun. 36:215-222.
58. Katayama, Y., T. Ito, and K. Hiramatsu. 2000. A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 44:1549-1555.
59. Kell, C. M., U. K. Sharma, C. G. Dowson, C. Town, T. S. Balganesh, and B. G. Spratt. 1993. Deletion analysis of the essentiality of penicillin-binding protein-1A, penicillin-binding protein-2B and penicillin-binding protein-2X of Streptococcus pneumoniae. FEMS Microbiol. Lett. 106:171-175.
60. Kopp, U., M. Roos, J. Wecke, and H. Labischinski. 1996. Staphylococcal peptidoglycan interpeptide bridge biosynthesis: a novel antistaphylococcal target? Microb. Drug Resist. 2:29-41.
61. Laible, G., and R. Hakenbeck. 1991. Five independent combinations of mutations can result in low-affinity penicillin-binding protein 2x of Streptococcus pneumoniae. J. Bacteriol. 173:6986-6990.
62. Ling, B. D., and B. Berger-Bächi. 1998. Increased overall antibiotic susceptibility in Staphylococcus aureus femAB null mutants. Antimicrob. Agents Chemother. 42:936-938.
63. Ma, X. X., T. Ito, C. Tiensasitorn, M. Jamklang, P. Chongtrakool, S. Boyle-Vavra, R. S. Daum, and K. Hiramatsu. 2002. Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob. Agents Chemother. 46:1147-1152.
64. Maidhof, H., B. Reinicke, P. Blümel, B. Berger-Bächi, and H. Labischinski. 1991. femA, which encodes a factor essential for expression of methicillin resistance, affects glycine content of peptidoglycan in methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. J. Bacteriol. 173:3507-3513.
65. Matsuhashi, M., C. Dietrich, and J. Strominger. 1965. Incorporation of glycine into the cell wall glycopeptide in Staphylococcus aureus: role of sRNA and lipid intermediates. Proc. Natl. Acad. Sci. USA 54:587-594.
66. Matsuhashi, M., C. P. Dietrich, and J. L. Strominger. 1967. Biosynthesis of the peptidoglycan of bacterial cell walls. III. The role of soluble ribonucleic acid and of lipid intermediates in glycine incorporation in Staphylococcus aureus. J. Biol. Chem. 242:3191-3206.
67. Mazmanian, S. K., G. Liu, H. Ton-That, and O. Schneewind. 1999. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760-763.
68. Mazmanian, S. K., H. Ton-That, K. Su, and O. Schneewind. 2002. An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc. Natl. Acad. Sci. USA 99:2293-2298.
69. Mouz, N., E. Gordon, A. M. Di Guilmi, I. Petit, Y. Petillot, Y. Dupont, R. Hakenbeck, T. Vernet, and O. Dideberg. 1998. Identification of a structural determinant for resistance to beta-lactam antibiotics in gram-positive bacteria. Proc. Natl. Acad. Sci. USA 95:13403-13406.
70. Murray, T., D. L. Popham, P. Setlow, A. M. Smith, K. P. Klugman, R. Hakenbeck, and J. Coyette. 1996. Identification and characterization of pbpC, the gene encoding Bacillus subtilis penicillin-binding protein 3. J. Bacteriol. 178:6001-6005.
71. Nakagawa, J., S. Tamaki, S. Tomioka, and M. Matsuhashi. 1984. Functional biosynthesis of cell wall peptidoglycan by polymorphic bifunctional polypeptides. Penicillin-binding protein 1Bs of Escherichia coli with activities of transglycosylase and transpeptidase. J. Biol. Chem. 259:13937-13946.
72. Navarre, W. W., and O. Schneewind. 1994. Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria. Mol. Microbiol. 14:115-121.
73. Navarre, W. W., and O. Schneewind. 1999. Surface proteins of grampositive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 63:174-229.
74. Novick, R. P. 1996. Possible alternatives to standard antibiotics in the management of infections with antibiotic-resistant organisms, p. 175-191. In C. F. Amabile-Cuevas (ed.), Antibiotic resistance: from molecular basics to therapeutic options. R. G. Landes Company, Austin, Tex.
75. Page, R. D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
76. Patti, J. M., and M. Höök. 1994. Microbial adhesins recognizing extracellular matrix macromolecules. Curr. Opin. Cell Biol. 6:752-758.
77. Perry, A. M., H. Ton-That, S. K. Mazmanian, and O. Schneewind. 2002. Anchoring of surface proteins to the cell wall of Staphylococcus aureus. III. Lipid II is an in vivo peptidoglycan substrate for sortase-catalyzed surface protein anchoring. J. Biol. Chem. 277:16241-16248.
78. Petinaki, E., G. Dimitracopoulos, and I. Spiliopoulou. 2001. Decreased affinity of PBP3 to methicillin in a clinical isolate of Staphylococcus epidermidis with borderline resistance to methicillin and free of the mecA gene. Microb. Drug Resist. 7:297-300.
79. Pinho, M. G., S. R. Filipe, H. de Lencastre, and A. Tomasz. 2001. Complementation of the essential peptidoglycan transpeptidase function of penicillin-binding protein 2 (PBP2) by the drug resistance protein PBP2A in Staphylococcus aureus. J. Bacteriol. 183:6525-6531.
80. Piras, G., D. Raze, A. el Kharroubi, D. Hastir, S. Engelbert, J. Coyette, and J. M. Ghuysen. 1993. Cloning and sequencing of the low-affinity penicillinbinding protein 3r-encoding gene of Enterococcus hirae S185: modular design and structural organization of the protein. J. Bacteriol. 175:2844-2852.
81. Pootoolal, J., M. G. Thomas, C. G. Marshall, J. M. Neu, B. K. Hubbard, C. T. Walsh, and G. D. Wright. 2002. Assembling the glycopeptide antibiotic scaffold: the biosynthesis of A47934 from Streptomyces toyocaensis NRRL15009. Proc. Natl. Acad. Sci. USA 99:8962-8967.
82. Raze, D., O. Dardenne, S. Hallut, M. Martinezbueno, J. Coyette, and J. M. Ghuysen. 1998. The gene encoding the low-affinity penicillin-binding protein 3r in Enterococcus hirae S185R is borne on a plasmid carrying other antibiotic resistance determinants. Antimicrob. Agents Chemother. 42:534-539.
83. Reichmann, P., A. Konig, J. Linares, F. Alcaide, F. C. Tenover, L. McDougal, S. Swidsinski, and R. Hakenbeck. 1997. A global gene pool for highlevel cephalosporin resistance in commensal Streptococcus species and Streptococcus pneumoniae. J. Infect. Dis. 176:1001-1012.
84. Rohrer, S., K. Ehlert, M. Tschierske, H. Labischinski, and B. Berger-Bächi. 1999. The essential Staphylococcus aureus gene fmhB is involved in the first step of peptidoglycan pentaglycine interpeptide formation. Proc. Natl. Acad. Sci. USA 96:9351-9356.
85. Ruzin, A., A. Severin, F. Ritacco, K. Tabei, G. Singh, P. A. Bradford, M. M. Siegel, S. J. Projan, D. M. Shlaes, A. M. Perry, H. Ton-That, S. K. Mazmanian, and O. Schneewind. 2002. Further evidence that a cell wall precursor [C(55)-MurNAc-(peptide)-GlcNAc] serves as an acceptor in a sorting reaction. J. Bacteriol. 184:2141-2147.
86. Ryffel, C., A. Strässle, F. H. Kayser, and B. Berger-Bächi. 1994. Mechanisms of heteroresistance in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 38:724-728.
87. Sauvage, E., F. Kerff, E. Fonzé, R. Hermann, B. Schoot, J.-P. Marquette, Y. Taburet, D. Prevost, J. Dumas, G. Leonard, P. Stefanic, J. Coyette, and P. Charlier. 2002. The 2.4 Å crystal structure of the penicillin-resistant penicillin-binding protein PBP5fm from Enterococcus faecium in complex with benzylpenicillin. Cell. Mol. Life Sci. 59:1223-1232.
88. Schleifer, K. H., and O. Kandler. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36:407-477.
89. Severin, A., A. M. Figueiredo, and A. Tomasz. 1996. Separation of abnormal cell wall composition from penicillin resistance through genetic transformation of Streptococcus pneumoniae. J. Bacteriol. 178:1788-1792.
90. Severin, A., and A. Tomasz. 1996. Naturally occurring peptidoglycan variants of Streptococcus pneumoniae. J. Bacteriol. 178:168-174.
91. Sifaoui, F., M. Arthur, L. Rice, and L. Gutmann. 2001. Role of penicillinbinding protein 5 in expression of ampicillin resistance and peptidoglycan structure in Enterococcus faecium. Antimicrob. Agents Chemother. 45:2594-2597.
92. Signoretto, C., M. Boaretti, and P. Canepari. 1998. Peptidoglycan synthesis by Enterococcus faecalis penicillin binding protein 5. Arch. Microbiol. 170:185-190.
93. Signoretto, C., P. Canepari, A. M. Perry, H. Ton-That, S. K. Mazmanian, and O. Schneewind. 2000. Paradoxical effect of inserting, in Enterococcus faecalis penicillin-binding protein 5, an amino acid box responsible for low affinity for penicillin in Enterococcus faecium. Arch. Microbiol. 173:213-219.
94. Simmonds, R. S., W. J. Simpson, and J. R. Tagg. 1997. Cloning and sequence analysis of zooA, a Streptococcus zooepidemicus gene encoding a bacteriocin-like inhibitory substance having a domain structure similar to that of lysostaphin. Gene 189:255-261.
95. Smith, A. M., and K. P. Klugman. 2001. Alterations in MurM, a cell wall muropeptide branching enzyme, increase high-level penicillin and cephalosporin resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 45:2393-2396.
96. Smith, A. M., K. P. Klugman, R. Hakenbeck, and J. Coyette. 2000. Nonpenicillin-binding protein mediated high-level penicillin and cephalosporin resistance in a Hungarian clone of Streptococcus pneumoniae. Microb. Drug Resist. 6:105-110.
97. Strominger, J., and J. Ghuysen. 1967. Mechanisms of enzymatic bacteriolysis. Cell walls of bacteria are solubilized by action of either specific carbohydrases or specific peptidases. Science 156:213-221.
98. Sugai, M. 1997. Peptidoglycan hydrolases of the staphylococci. J. Infect. Chemother. 3:113-127.
99. Sugai, M., T. Fujiwara, H. Komatsuzawa, and H. Suginaka. 1998. Identification and molecular characterization of a gene homologous to epr (endopeptidase resistance gene) in Staphylococcus aureus. Gene 224:67-75.
100. Sugai, M., T. Fujiwara, K. Ohta, H. Komatsuzawa, M. Ohara, and H. Suginaka. 1997. epr, which encodes glycylglycine endopeptidase resistance, is homologous to femAB and affects serine content of peptidoglycan cross bridges in Staphylococcus capitis and Staphylococcus aureus. J. Bacteriol. 179:4311-4318.
101. Sugai, M., S. Yamada, S. Nakashima, H. Komatsuzawa, A. Matsumoto, T. Oshida, and H. Suginaka. 1997. Localized perforation of the cell wall by a major autolysin: atl gene products and the onset of penicillin-induced lysis of Staphylococcus aureus. J. Bacteriol. 179:2958-2962.
102. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
103. Thumm, G., and F. Götz. 1997. Studies on prolysostaphin processing and characterization of the lysostaphin immunity factor (Lif) of Staphylococcus simulans biovar staphylolyticus. Mol. Microbiol. 23:1251-1265.
104. Tipper, D., and J. Strominger. 1965. Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine. Proc. Natl. Acad. Sci. USA 54:1133.
105. Tomasz, A. 1986. Penicillin-binding proteins and the antibacterial effectiveness of beta-lactam antibiotics. Rev. Infect. Dis. 8(Suppl. 3):S260-S278.
106. Tomasz, A., H. B. Drugeon, H. M. de Lencastre, D. Jabes, and L. McDougall. 1989. New mechanism for methicillin resistance in Staphylococcus aureus: clinical isolates that lack the PBP2a gene and contain normal penicillin-binding proteins with modified penicillin-binding capacity. Antimicrob. Agents Chemother. 33:1869-1874.
107. Ton-That, H., H. Labischinski, B. Berger-Bächi, and O. Schneewind. 1998. Anchor structure of staphylococcal surface proteins. III. Role of the femA, femB, and femX factors in anchoring surface proteins to the bacterial cell wall. J. Biol. Chem. 273:29143-29149.
108. Tschierske, M., K. Ehlert, A. M. Stranden, and B. B. Berger. 1997. Lif, the lysostaphin immunity factor, complements FemB in staphylococcal peptidoglycan interpeptide bridge formation. FEMS Microbiol. Lett. 153:261-264.
109. Tschierske, M., C. Mori, S. Rohrer, K. Ehlert, K. J. Shaw, and B. BergerBächi. 1999. Identification of three additional femAB-like open reading frames in Staphylococcus aureus. FEMS Microbiol. Lett. 171:97-102.
110. Umemoto, T., T. Ota, H. Sagawa, K. Kato, H. Takada, M. Tsujimoto, A. Kawasaki, T. Ogawa, K. Harada, and S. Kotani. 1981. Chemical and biological properties of a peptidoglycan isolated from Treponema pallidum kazan. Infect. Immun. 31:767-774.
111. van Heijenoort, J. 1994. Biosynthesis of the bacterial peptidoglycan unit. In J.-M. Ghuysen and R. Hakenbeck (ed.), Bacterial cell wall. Elsevier Science B.V., Amsterdam, The Netherlands.
112. Vannuffel, P., M. Hersterspreute, M. Bouyer, B. Vandercam, M. Philippe, and J.-L. Gala. 1999. Molecular characterization of femA from Staphylococcus hominis and Staphylococcus saprophyticus, and femA-based discrimination of staphylococcal species. Res. Microbiol. 150:129-141.
113. Wang, J. E., P. F. Jorgensen, M. Almlof, C. Thiemermann, S. J. Foster, A. O. Aasen, and R. Solberg. 2000. Peptidoglycan and lipoteichoic acid from Staphylococcus aureus induce tumor necrosis factor alpha, interleukin 6 (IL-6), and IL-10 production in both T cells and monocytes in a human whole blood model. Infect. Immun. 68:3965-3970.
114. Weber, B., K. Ehlert, A. Diehl, P. Reichmann, H. Labischinski, and R. Hakenbeck. 2000. Thefib locus in Streptococcus pneumoniae is required for peptidoglycan crosslinking and PBP-mediated β-lactam resistance. FEMS Microbiol. Lett. 188:81-85.
115. Yanagihara, Y., K. Kamisango, S. Yasuda, S. Kobayashi, I. Mifuchi, I. Azuma, Y. Yamamura, and R. Johnson. 1984. Chemical compositions of cell walls and polysaccharide fractions of spirochetes. Microbiol. Immunol. 28:535-544.
116. Yoshimura, A., E. Lien, R. R. Ingalls, E. Tuomanen, R. Dziarski, and D. Golenbock. 1999. Cutting edge: recognition of gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163:1-5.
117. Zhao, G., W. K. Yeh, R. H. Carnahan, J. Flokowitsch, T. I. Meier, W. E. Alborn, Jr., G. W. Becker, S. R. Jaskunas, A. M. Smith, K. P. Klugman, R. Hakenbeck, and J. Coyette. 1997. Biochemical characterization of penicillin-resistant and -sensitive penicillin-binding protein 2x transpeptidase activities of Streptococcus pneumoniae and mechanistic implications in bacterial resistance to beta-lactam antibiotics. J. Bacteriol. 179:4901-4908.