Genetics of peptidoglycan biosynthesis

Microbiology Spectrum

Volumn 2, Issue 4, 2014, Pages

  Pavelka, Martin S ^a   Mahapatra, Sebabrata ^b   Crick, Dean C ^b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b Department of Ecosystem Science and Sustainability   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BETA LACTAM; PEPTIDOGLYCAN;

BIOSYNTHESIS; DRUG EFFECTS; GENETICS; METABOLISM; MYCOBACTERIUM;

ANTI-BACTERIAL AGENTS; BETA-LACTAMS; BIOSYNTHETIC PATHWAYS; MYCOBACTERIUM; PEPTIDOGLYCAN;

EID: 84907508667     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.MGM2-0034-2013     Document Type: Article

References (155)

1. Lederer E. 1971. The mycobacterial cell wall. Pure Appl Chem 25:135-165.
2. Mahapatra S, Basu J, Brennan PJ, Crick DC. 2005. Structure, biosynthesis, and genetics of the mycolic acid-arabinogalactan-peptidoglycan complex, p 275-277. In Cole ST, Eisenbach KD, McMurray DN, Jacobs WR Jr (eds), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC.
3. Schleifer KH, Kandler O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407-477.
4. Azuma I, Thomas DW, Adam A, Ghuysen JM, Bonaly R, Petit JF, Lederer E. 1970. Occurrence of N-glycolylmuramic acid in bacterial cell walls. A preliminary survey. Biochim Biophys Acta 208:444-451.
5. Mahapatra S, SchermanH, Brennan PJ, CrickDC. 2005.Nglycolylation of the nucleotide precursors of peptidoglycan biosynthesis of Mycobacterium spp. is altered by drug treatment. J Bacteriol 187:2341-2347.
6. Mahapatra S, Crick DC, McNeil MR, Brennan PJ. 2008. Unique structural features of the peptidoglycan of Mycobacterium leprae. J Bacteriol 190:655-661.
7. Mahapatra S, Yagi T, Belisle JT, Espinosa BJ, Hill PJ, McNeil MR, Brennan PJ, Crick DC. 2005. Mycobacterial lipid II is composed of a complex mixture of modified muramyl and peptide moieties linked to decaprenyl phosphate. J Bacteriol 187:2747-2757.
8. Raymond JB, Mahapatra S, Crick DC, Pavelka MS Jr. 2005. Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J Biol Chem 280:326-333.
9. Coulombe F, Divangahi M, Veyrier F, de Leseleuc L, Gleason JL, Yang Y, Kelliher MA, Pandey AK, Sassetti CM, Reed MB, Behr MA. 2009. Increased NOD2-mediated recognition of N-glycolyl muramyl dipeptide. J Exp Med 206:1709-1716.
10. Goffin C, Ghuysen JM. 2002. Biochemistry and comparative genomics of SxxK superfamily acyltransferases offer a clue to the mycobacterial paradox: presence of penicillin-susceptible target proteins versus lack of efficiency of penicillin as therapeutic agent. Microbiol Mol Biol Rev 66:702-738.
11. Lavollay M, Arthur M, Fourgeaud M, Dubost L, Marie A, Riegel P, Gutmann L, Mainardi JL. 2009. The beta-lactam-sensitive D, D-carboxypeptidase activity of Pbp4 controls the L, D and D, D transpeptidation pathways in Corynebacterium jeikeium. Mol Microbiol 74:650-661.
12. Lavollay M, Arthur M, Fourgeaud M, Dubost L, Marie A, Veziris N, Blanot D, Gutmann L, Mainardi JL. 2008. The peptidoglycan of stationary phase Mycobacterium tuberculosis predominantly contains cross-links generated by L, D-transpeptidation. J Bacteriol 190:4360-4366
13. Mainardi JL, Fourgeaud M, Hugonnet JE, Dubost L, Brouard JP, Ouazzani J, Rice LB, Gutmann L, Arthur M. 2005. A novel peptidoglycan cross-linking enzyme for a beta-lactam-resistant transpeptidation pathway. J Biol Chem 280:38146-38152.
14. Mainardi JL, Hugonnet JE, Rusconi F, Fourgeaud M, Dubost L, Moumi AN, Delfosse V, Mayer C, Gutmann L, Rice LB, Arthur M. 2007. Unexpected inhibition of peptidoglycan L, D-transpeptidase from Enterococcus faecium by the beta-lactam imipenem. J Biol Chem 282:30414-30422.
15. Mainardi JL, Legrand R, Arthur M, Schoot B, van Heijenoort J, Gutmann L. 2000. Novel mechanism of beta-lactam resistance due to bypass of D, D-transpeptidation in Enterococcus faecium. J Biol Chem 275:16490-16496.
16. Sanders AN, Pavelka MS. 2013. Phenotypic analysis of Eschericia coli mutants lacking L, D-transpeptidases. Microbiology 159:1842-1852.
17. Magnet S, Arbeloa A, Mainardi JL, Hugonnet JE, Fourgeaud M, Dubost L, Marie A, Delfosse V, Mayer C, Rice LB, Arthur M. 2007. Specificity of L, D-transpeptidases from Gram-positive bacteria producing different peptidoglycan chemotypes. J Biol Chem 282:13151-13159.
18. Quintela JC, Caparros M, de Pedro MA. 1995. Variability of peptidoglycan structural parameters in gram-negative bacteria. FEMS Microbiol Lett 125:95-100.
19. Wietzerbin J, Das BC, Petit J-F, Lederer E, Leyh-Bouille M, Ghuysen J-M. 1974. Occurence of D-alanyl-(D)-meso-diaminopimelic acid and meso-diaminopimelyl-meso-diaminopimelic acid interpeptide linkages in the peptidoglycan of mycobacteria. Biochemistry 13:3471-3476.
20. Kumar P, Arora K, Lloyd JR, Lee IY, Nair V, Fischer E, Boshoff HI, Barry CE, 3rd. 2012. Meropenem inhibits D, D-carboxypeptidase activity in Mycobacterium tuberculosis. Mol Microbiol 86:367-381.
21. Lavollay M, Fourgeaud M, Herrmann JL, Dubost L, Marie A, Gutmann L, Arthur M, Mainardi JL. 2011. The peptidoglycan of Mycobacterium abscessus is predominantly cross-linked by L, D-transpeptidases. J Bacteriol 193:778-782.
22. McNeil M, Daffe M, Brennan PJ. 1990. Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J Biol Chem 265:18200-18206.
23. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
24. Slayden RA, Jackson M, Zucker J, Ramirez MV, Dawson CC, Crew R, Sampson NS, Thomas ST, Jamshidi N, Sisk P, Caspi R, Crick DC, McNeil MR, Pavelka MS, Niederweis M, Siroy A, Dona V, McFadden J, Boshoff H, Lew JM. 2013. Updating and curating metabolic pathways of TB. Tuberculosis 93:47-59.
25. Cirillo JD, Weisbrod TR, Pascopella L, Jacobs WR Jr. 1994. Isolation and characterization of the aspartate semialdehyde dehydrogenase and aspartokinase genes from mycobacteria. Mol Microbiol 11:629-639.
26. Pavelka MS Jr, Weisbrod TR, Jacobs WR Jr. 1997. Cloning of the dapB gene, encoding dihydrodipicolinate reductase, from Mycobacterium tuberculosis. J Bacteriol 179:2777-2782.
27. Jha RK, Katagihallimath N, Hota SK, Das KS, de Sousa SM. 2012. An assay for exogenous sources of purified MurG, enabled by the complementation of Escherichia coli murG(Ts) by the Mycobacterium tuberculosis homologue. FEMS Microbiol Lett 326:161-167.
28. van Heijenoort J. 1998. Assembly of the monomer unit of bacterial peptidoglycan. Cell Mol Life Sci 54:300-304.
29. Ashiuchi M, Kuwana E, Komatsu K, Soda K, Misono H. 2003. Differences in effects on DNA gyrase activity between two glutamate racemases of Bacillus subtilis, the poly-gamma-glutamate synthesislinking Glr enzyme and the YrpC (MurI) isozyme. FEMS Microbiol Lett 223:221-225.
30. Sengupta S, Ghosh S, Nagaraja V. 2008. Moonlighting function of glutamate racemase from Mycobacterium tuberculosis: racemization and DNA gyrase inhibition are two independent activities of the enzyme. Microbiology 154:2796-2803.
31. Umbarger HE. 1978. Amino acid biosynthesis and its regulation. Annu Rev Biochem 47:533-606.
32. Pavelka MS Jr, Jacobs WR Jr. 1996. Biosynthesis of diaminopimelate (DAP), the precursor of lysine and a component of the peptidoglycan, is an essential function of Mycobacterium smegmatis. J Bacteriol 178:6496-6507.
33. Consaul SA, Jacobs WR Jr, Pavelka MS Jr. 2003. Extragenic suppression of the requirement for diaminopimelate in diaminopimelate auxotrophs of Mycobacterium smegmatis. FEMS Microbiol Lett 225: 131-135.
34. Consaul SA, Wright LF, Mahapatra S, Crick DC, Pavelka MS Jr. 2005. An unusual mutation results in the replacement of diaminopimelate with lanthionine in the peptidoglycan of a mutant strain of Mycobacterium smegmatis. J Bacteriol 187:1612-1620.
35. Mengin-Lecreulx D, Blanot D, van Heijenoort J. 1994. Replacement of diaminopimelic acid by cystathionine or lanthionine in the peptidoglycan of Escherichia coli. J Bacteriol 176:4321-4327.
36. Flores AR, Parsons LM, Pavelka MS Jr. 2005. Characterization of novel Mycobacterium tuberculosis and Mycobacterium smegmatis mutants hypersusceptible to beta-lactam antibiotics. J Bacteriol 187: 1892-1900.
37. Pavelka MS Jr, Jacobs WR Jr. 1999. Comparison of the construction of unmarked deletion mutations in Mycobacterium smegmatis, Mycobacterium bovis bacillus Calmette-Guerin, and Mycobacterium tuberculosis H37Rv by allelic exchange. J Bacteriol 181:4780-4789.
38. Liu L, Yoshimura T, Endo K, Kishimoto K, Fuchikami Y, Manning JM, Esaki N, Soda K. 1998. Compensation for D-glutamate auxotrophy of Escherichia coli WM335 by D-amino acid aminotransferase gene and regulation of murI expression. Biosci Biotechnol Biochem 62:193-195.
39. Chacon O, Feng Z, Harris NB, Caceres NE, Adams LG, Barletta RG. 2002. Mycobacterium smegmatis D-alanine racemase mutants are not dependent on D-alanine for growth. Antimicrobial Agents Chemother 46:47-54.
40. Awasthy D, Bharath S, Subbulakshmi V, Sharma U. 2012. Alanine racemase mutants of Mycobacterium tuberculosis require D-alanine for growth and are defective for survival in macrophages and mice. Microbiology 158:319-327.
41. Milligan DL, Tran SL, Strych U, Cook GM, Krause KL. 2007. The alanine racemase of Mycobacterium smegmatis is essential for growth in the absence of D-alanine. J Bacteriol 189:8381-8386.
42. Feng Z, Barletta RG. 2003. Roles of Mycobacterium smegmatis D-alanine:D-alanine ligase and D-alanine racemase in the mechanisms of action of and resistance to the peptidoglycan inhibitor D-cycloserine. Antimicrobial Agents Chemother 47:283-291.
43. van Heijenoort J. 2001. Recent advances in the formation of the bacterial peptidoglycan monomer unit. Nat Prod Rep 18:503-519.
44. van Heijenoort J. 2001. Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11:25R-36R.
45. Mengin-Lecreulx D, Flouret B, van Heijenoort J. 1982. Cytoplasmic steps of peptidoglycan synthesis in Escherichia coli. J Bacteriol 151:1109-1117.
46. De Smet KA, Kempsell KE, Gallagher A, Duncan K, Young DB. 1999. Alteration of a single amino acid residue reverses fosfomycin resistance of recombinant MurA from Mycobacterium tuberculosis. Microbiology 145:3177-3184.
47. Eschenburg S, Priestman M, Schonbrunn E. 2005. Evidence that the fosfomycin target Cys115 in UDP-N-acetylglucosamine enolpyruvyl transferase (MurA) is essential for product release. J Biol Chem280:3757-3763.
48. Kumar V, Saravanan P, Arvind A, Mohan CG. 2011. Identification of hotspot regions of MurB oxidoreductase enzyme using homology modeling, molecular dynamics and molecular docking techniques. J Mol Model 17:939-953.
49. Sassetti CM, Boyd DH, Rubin EJ. 2001. Comprehensive identification of conditionally essential genes in mycobacteria. Proc Natl Acad Sci USA 98:12712-12717.
50. Mengin-Lecreulx D, van Heijenoort J, Park JT. 1996. Identification of the mpl gene encoding UDP-N-acetylmuramate: L-alanyl-gamma-dglutamyl-meso-diaminopimelate ligase in Escherichia coli and its role in recycling of cell wall peptidoglycan. J Bacteriol 178:5347-5352.
51. Mahapatra S, Crick DC, Brennan PJ. 2000. Comparison of the UDPN-acetylmuramate:L-alanine ligase enzymes from Mycobacterium tuberculosis and Mycobacterium leprae. J Bacteriol 182:6827-6830.
52. Munshi T, Gupta A, Evangelopoulos D, Guzman JD, Gibbons S, Keep NH, Bhakta S. 2013. Characterisation of ATP-dependent Mur ligases involved in the biogenesis of cell wall peptidoglycan in Mycobacterium tuberculosis. PLoS One 8:e60143.
53. Draper P. 1976. Cell walls of Mycobacterium leprae. Int J Lepr Other Mycobact Dis 44:95-98.
54. Barreteau H, Sosic I, Turk S, Humljan J, Tomasic T, Zidar N, Herve M, Boniface A, Peterlin-Masic L, Kikelj D, Mengin-Lecreulx D, Gobec S, Blanot D. 2012. MurD enzymes from different bacteria: evaluation of inhibitors. Biochem Pharmacol 84:625-632.
55. Basavannacharya C, Robertson G, Munshi T, Keep NH, Bhakta S. 2010. ATP-dependent MurE ligase in Mycobacterium tuberculosis: biochemical and structural characterisation. Tuberculosis 90:16-24.
56. Bernard E, Rolain T, Courtin P, Hols P, Chapot-Chartier MP. 2011. Identification of the amidotransferase AsnB1 as being responsible for meso-diaminopimelic acid amidation in Lactobacillus plantarum peptidoglycan. J Bacteriol 193:6323-6330.
57. Figueiredo TA, Sobral RG, Ludovice AM, Almeida JM, Bui NK, Vollmer W, de Lencastre H, Tomasz A. 2012. Identification of genetic determinants and enzymes involved with the amidation of glutamic acid residues in the peptidoglycan of Staphylococcus aureus. PLoS Pathog 8: e1002508.
58. Munch D, Roemer T, Lee SH, Engeser M, Sahl HG, Schneider T. 2012. Identification and in vitro analysis of the GatD/MurT enzymecomplex catalyzing lipid II amidation in Staphylococcus aureus. PLoS Pathog 8:e1002509.
59. Menon AK. 1995. Flippases. Trends Cell Biol 5:355-360.
60. Pomorski T, Holthuis JC, Herrmann A, van Meer G. 2004. Tracking down lipid flippases and their biological functions. J Cell Sci 117:805-813.
61. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635-700.
62. Weppner WA, Neuhaus FC. 1978. Biosynthesis of peptidoglycan. Definition of the microenvironment of undecaprenyl diphosphate-Nacetylmuramyl-( 5-dimethylaminonaphthalene-1-sulfonyl) pentapeptide by fluorescence spectroscopy. J Biol Chem 253:472-478.
63. van Dam V, Sijbrandi R, Kol M, Swiezewska E, de Kruijff B, Breukink E. 2007. Transmembrane transport of peptidoglycan precursors across model and bacterial membranes. Mol Microbiol 64:1105-1114.
64. Siewert G, Strominger JL. 1967. Bacitracin: an inhibitor of the dephosphorylation of lipid pyrophosphate, an intermediate in the biosynthesis of the peptidoglycan of bacterial cell walls. Proc Natl Acad Sci USA 57:767-773.
65. Bosne-David S, Barros V, Verde SC, Portugal C, David HL. 2000. Intrinsic resistance of Mycobacterium tuberculosis to clarithromycin is effectively reversed by subinhibitory concentrations of cell wall inhibitors. J Antimicrob Chemother 46:391-395.
66. Inoue A, Murata Y, Takahashi H, Tsuji N, Fujisaki S, Kato J. 2008. Involvement of an essential gene, mviN, in murein synthesis in Escherichia coli. J Bacteriol 190:7298-7301.
67. Mohammadi T, van Dam V, Sijbrandi R, Vernet T, Zapun A, Bouhss A, Diepeveen-de Bruin M, Nguyen-Disteche M, de Kruijff B, Breukink E. 2011. Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J 30:1425-1432.
68. Ruiz N. 2008. Bioinformatics identification of MurJ (MviN) as the peptidoglycan lipid II flippase in Escherichia coli. Proc Natl Acad Sci USA 105:15553-15557.
69. Gee CL, Papavinasasundaram KG, Blair SR, Baer CE, Falick AM, King DS, Griffin JE, Venghatakrishnan H, Zukauskas A, Wei JR, Dhiman RK, Crick DC, Rubin EJ, Sassetti CM, Alber T. 2012. A phosphorylated pseudokinase complex controls cell wall synthesis in mycobacteria. Sci Signal 5:ra7.
70. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C. 2011. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39:D561-D568.
71. Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier MH Jr. 2003. The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem 270:799-813.
72. Liu D, Cole RA, Reeves PR. 1996. An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J Bacteriol 178:2102-2107.
73. Rick PD, Barr K, Sankaran K, Kajimura J, Rush JS, Waechter CJ. 2003. Evidence that the wzxE gene of Escherichia coli K-12 encodes a protein involved in the transbilayer movement of a trisaccharide-lipid intermediate in the assembly of enterobacterial common antigen. J Biol Chem 278:16534-16542.
74. Ma Y, Stern RJ, Scherman MS, Vissa VD, Yan W, Jones VC, Zhang F, Franzblau SG, Lewis WH, McNeil MR. 2001. Drug targeting Mycobacterium tuberculosis cell wall synthesis: genetics of dTDP-rhamnose synthetic enzymes and development of a microtiter plate-based screen for inhibitors of conversion of dTDP-glucose to dTDP-rhamnose. Antimicrob Agents Chemother 45:1407-1416.
75. Hancock IC, Carman S, Besra GS, Brennan PJ, Waite E. 2002. Ligation of arabinogalactan to peptidoglycan in the cell wall of Mycobacterium smegmatis requires concomitant synthesis of the two wall polymers. Microbiology 148:3059-3067.
76. Yagi T, Mahapatra S, Mikusova K, Crick DC, Brennan PJ. 2003. Polymerization of mycobacterial arabinogalactan and ligation to peptidoglycan. J Biol Chem 278:26497-26504.
77. Goffin C, Ghuysen JM. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol Mol Biol Rev 62:1079-1093.
78. Basu J, Mahapatra S, Kundu M, Mukhopadhyay S, Nguyen-Disteche M, Dubois P, Joris B, Van Beeumen J, Cole ST, Chakrabarti P, Ghuysen JM. 1996. Identification and overexpression in Escherichia coli of a Mycobacterium leprae gene, pon1, encoding a high-molecular-mass class A penicillin-binding protein, PBP1. J Bacteriol 178:1707-1711.
79. Mahapatra S, Bhakta S, Ahamed J, Basu J. 2000. Characterization of derivatives of the high-molecular-mass penicillin-binding protein (PBP) 1 of Mycobacterium leprae. Biochem J 350(Pt 1):75-80.
80. Billman-Jacobe H, Haites RE, Coppel RL. 1999. Characterization of a Mycobacterium smegmatis mutant lacking penicillin binding protein 1. Antimicrob Agents Chemother 43:3011-3013.
81. Hett EC, Chao MC, Rubin EJ. 2010. Interaction and modulation of two antagonistic cell wall enzymes of mycobacteria. PLoS Pathog 6: e1001020.
82. Prisic S, Dankwa S, Schwartz D, Chou MF, Locasale JW, Kang CM, Bemis G, Church GM, Steen H, Husson RN. 2010. Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proc Nat Acad Sci USA 107:7521-7526.
83. Keer J, Smeulders MJ, Gray KM, Williams HD. 2000. Mutants of Mycobacterium smegmatis impaired in stationary-phase survival. Microbiology 146(Pt 9):2209-2217.
84. Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S. 2008. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 14:849-854.
85. Vandal OH, Roberts JA, Odaira T, Schnappinger D, Nathan CF, Ehrt S. 2009. Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J Bacteriol 191:625-631.
86. Patru MM, Pavelka MS Jr. 2010. A role for the class A penicillinbinding protein PonA2 in the survival of Mycobacterium smegmatis under conditions of nonreplication. J Bacteriol 192:3043-3054.
87. Dutta NK, Mehra S, Didier PJ, Roy CJ, Doyle LA, Alvarez X, Ratterree M, Be NA, Lamichhane G, Jain SK, Lacey MR, Lackner AA, Kaushal D. 2010. Genetic requirements for the survival of tubercle bacilli in primates. J Infect Dis 201:1743-1752.
88. Bourai N, Jacobs WR Jr, Narayanan S. 2012. Deletion and overexpression studies on DacB2, a putative low molecular mass penicillin binding protein from Mycobacterium tuberculosis H(37)Rv. Microb Pathog 52:109-116.
89. Magnet S, Dubost L, Marie A, Arthur M, Gutmann L. 2008. Identification of the L, D-transpeptidases for peptidoglycan cross-linking in Escherichia coli. J Bacteriol 190:4782-4785.
90. Magnet S, Bellais S, Dubost L, Fourgeaud M, Mainardi JL, Petit-Frere S, Marie A, Mengin-Lecreulx D, Arthur M, Gutmann L. 2007. Identification of the L, D-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J Bacteriol 189:3927-3931.
91. Dramsi S, Magnet S, Davison S, Arthur M. 2008. Covalent attachment of proteins to peptidoglycan. FEMS Microbiol Rev 32:307-320.
92. Gupta R, Lavollay M, Mainardi JL, Arthur M, Bishai WR, Lamichhane G. 2010. The Mycobacterium tuberculosis protein LdtMt2 is a nonclassical transpeptidase required for virulence and resistance to amoxicillin. Nat Med 16:466-469.
93. Purdy GE, Niederweis M, Russell DG. 2009. Decreased outer membrane permeability protects mycobacteria from killing by ubiquitinderived peptides. Mol Microbiol 73:844-857.
94. Park JT, Uehara T. 2008. How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol Mol Biol Rev 72:211-227.
95. Deng LL, Humphries DE, Arbeit RD, Carlton LE, Smole SC, Carroll JD. 2005. Identification of a novel peptidoglycan hydrolase CwlM in Mycobacterium tuberculosis. Biochim Biophys Acta 1747:57-66.
96. Mahapatra S, Piechota C, Gil F, Ma Y, Huang H, Scherman MS, Jones V, Pavelka MS Jr, Moniz-Pereira J, Pimentel M, McNeil MR, Crick DC. 2013. Mycobacteriophage Ms6 LysA: a peptidoglycan amidase and a useful analytical tool. Appl Environ Microbiol 79:768-773.
97. Mukamolova GV, Kaprelyants AS, Young DI, Young M, Kell DB. 1998. A bacterial cytokine. Proc Natl Acad Sci USA 95:8916-8921.
98. Mukamolova GV, Turapov OA, Young DI, Kaprelyants AS, Kell DB, Young M. 2002. A family of autocrine growth factors in Mycobacterium tuberculosis. Mol Microbiol 46:623-635.
99. Kana BD, Mizrahi V. 2010. Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling. FEMS Immunol Med Microbiol 58:39-50.
100. Zhu W, Plikaytis BB, Shinnick TM. 2003. Resuscitation factors from mycobacteria: homologs of Micrococcus luteus proteins. Tuberculosis (Edinb) 83:261-269.
101. Mukamolova GV, Kormer SS, Kell DB, Kaprelyants AS. 1999. Stimulation of the multiplication of Micrococcus luteus by an autocrine growth factor. Arch Microbiol 172:9-14.
102. Mukamolova GV, Murzin AG, Salina EG, Demina GR, Kell DB, Kaprelyants AS, Young M. 2006. Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol Microbiol 59:84-98.
103. Mukamolova GV, Turapov OA, Kazarian K, Telkov M, Kaprelyants AS, Kell DB, Young M. 2002. The rpf gene of Micrococcus luteus encodes an essential secreted growth factor. Mol Microbiol 46:611-621.
104. Shleeva M, Mukamolova GV, Young M, Williams HD, Kaprelyants AS. 2004. Formation of "non-culturable" cells of Mycobacterium smegmatis in stationary phase in response to growth under suboptimal conditions and their Rpf-mediated resuscitation. Microbiology 150:1687-1697.
105. Shleeva MO, Bagramyan K, Telkov MV, Mukamolova GV, Young M, Kell DB, Kaprelyants AS. 2002. Formation and resuscitation of "nonculturable" cells of Rhodococcus rhodochrous and Mycobacterium tuberculosis in prolonged stationary phase. Microbiology 148:1581-1591.
106. Kana BD, Gordhan BG, Downing KJ, Sung N, Vostroktunova G, Machowski EE, Tsenova L, Young M, Kaprelyants A, Kaplan G, Mizrahi V. 2008. The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol Microbiol 67:672-684.
107. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honore N, Garnier T, Churcher C, Harris D, Mungall K, Basham D, Brown D, Chillingworth T, Connor R, Davies RM, Devlin K, Duthoy S, Feltwell T, Fraser A, Hamlin N, Holroyd S, Hornsby T, Jagels K, Lacroix C, Maclean J, Moule S, Murphy L, Oliver K, Quail MA, Rajandream MA, Rutherford KM, Rutter S, Seeger K, Simon S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Taylor K, Whitehead S, Woodward JR, Barrell BG. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007-1011.
108. Tufariello JM, Jacobs WR Jr, Chan J. 2004. Individual Mycobacterium tuberculosis resuscitation-promoting factor homologues are dispensable for growth in vitro and in vivo. Infect Immun 72:515-526.
109. Downing KJ, Betts JC, Young DI, McAdam RA, Kelly F, Young M, Mizrahi V. 2004. Global expression profiling of strains harbouring null mutations reveals that the five rpf-like genes of Mycobacterium tuberculosis show functional redundancy. Tuberculosis (Edinb) 84:167-179.
110. Tufariello JM, Mi K, Xu J, Manabe YC, Kesavan AK, Drumm J, Tanaka K, Jacobs WR Jr, Chan J. 2006. Deletion of the Mycobacterium tuberculosis resuscitation-promoting factor Rv1009 gene results in delayed reactivation from chronic tuberculosis. Infect Immun 74:2985-2995.
111. Biketov S, Potapov V, Ganina E, Downing K, Kana BD, Kaprelyants A. 2007. The role of resuscitation promoting factors in pathogenesis and reactivation of Mycobacterium tuberculosis during intra-peritoneal infection in mice. BMC Infect Dis 7:146.
112. Downing KJ, Mischenko VV, Shleeva MO, Young DI, Young M, Kaprelyants AS, Apt AS, Mizrahi V. 2005. Mutants of Mycobacterium tuberculosis lacking three of the five rpf-like genes are defective for growth in vivo and for resuscitation in vitro. Infect Immun 73:3038-3043.
113. Russell-Goldman E, Xu J, Wang X, Chan J, Tufariello JM. 2008. A Mycobacterium tuberculosis Rpf double-knockout strain exhibits profound defects in reactivation from chronic tuberculosis and innate immunity phenotypes. Infect Immun 76:4269-4281.
114. Kondratieva T, Rubakova E, Kana BD, Biketov S, Potapov V, Kaprelyants A, Apt A. 2011. Mycobacterium tuberculosis attenuated by multiple deletions of rpf genes effectively protects mice against TB infection. Tuberculosis 91:219-223.
115. Anantharaman V, Aravind L. 2003. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol 4:R11.
116. Wuenscher MD, Kohler S, Bubert A, Gerike U, GoebelW. 1993. The iap gene of Listeria monocytogenes is essential for cell viability, and its gene product, p60, has bacteriolytic activity. J Bacteriol 175:3491-3501.
117. Gao LY, Pak M, Kish R, Kajihara K, Brown EJ. 2006. A mycobacterial operon essential for virulence in vivo and invasion and intracellular persistence in macrophages. Infection Immun 74:1757-1767.
118. Both D, Schneider G, Schnell R. 2011. Peptidoglycan remodeling in Mycobacterium tuberculosis: comparison of structures and catalytic activities of RipA and RipB. J Mol Biol 413:247-260.
119. Hett EC, Chao MC, Steyn AJ, Fortune SM, Deng LL, Rubin EJ. 2007. A partner for the resuscitation-promoting factors of Mycobacterium tuberculosis. Mol Microbiol 66:658-668.
120. Hett EC, Chao MC, Deng LL, Rubin EJ. 2008. A mycobacterial enzyme essential for cell division synergizes with resuscitation-promoting factor. PLoS Pathog 4:e1000001.
121. Chao MC, Kieser KJ, Minami S, Mavrici D, Aldridge BB, Fortune SM, Alber T, Rubin EJ. 2013. Protein complexes and proteolytic activation of the cell wall hydrolase RipA regulate septal resolution in mycobacteria. PLoS Pathog 9:e1003197.
122. Parthasarathy G, Lun S, Guo H, Ammerman NC, Geiman DE, Bishai WR. 2012. Rv2190c, an NlpC/P60 family protein, is required for full virulence of Mycobacterium tuberculosis. PLoS One 7:e43429.
123. Piuri M, Hatfull GF. 2006. A peptidoglycan hydrolase motif within the mycobacteriophage TM4 tape measure protein promotes efficient infection of stationary phase cells. Mol Microbiol 62:1569-1585.
124. Datta P, Dasgupta A, Singh AK, Mukherjee P, Kundu M, Basu J. 2006. Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol 62:1655-1673.
125. Mukherjee P, Sureka K, Datta P, Hossain T, Barik S, Das KP, Kundu M, Basu J. 2009. Novel role of Wag31 in protection of mycobacteria under oxidative stress. Mol Microbiol 73:103-119.
126. Hamasha K, Sahana MB, Jani C, Nyayapathy S, Kang CM, Rehse SJ. 2010. The effect of Wag31 phosphorylation on the cells and the cell envelope fraction of wild-type and conditional mutants of Mycobacterium smegmatis studied by visible-wavelength Raman spectroscopy. Biochem Biophys Res Commun 391:664-668.
127. Jani C, Eoh H, Lee JJ, Hamasha K, Sahana MB, Han JS, Nyayapathy S, Lee JY, Suh JW, Lee SH, Rehse SJ, Crick DC, Kang CM. 2010. Regulation of polar peptidoglycan biosynthesis by Wag31 phosphorylation in mycobacteria. BMC Microbiol 10:327.
128. Kang CM, Nyayapathy S, Lee JY, Suh JW, Husson RN. 2008. Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. Microbiology 154:725-735.
129. Dasgupta A, Datta P, Kundu M, Basu J. 2006. The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 152: 493-504.
130. Fedarovich A, Nicholas RA, Davies C. 2010. Unusual conformation of the SxN motif in the crystal structure of penicillin-binding protein A from Mycobacterium tuberculosis. J Mol Biol 398:54-65.
131. Fedarovich A, Nicholas RA, Davies C. 2012. The role of the beta5-alpha11 loop in the active-site dynamics of acylated penicillin-binding protein A from Mycobacterium tuberculosis. J Mol Biol 418:316-330.
132. Kiran M, Chauhan A, Dziedzic R, Maloney E, Mukherji SK, Madiraju M, Rajagopalan M. 2009. Mycobacterium tuberculosis ftsH expression in response to stress and viability. Tuberculosis 89(Suppl 1): S70-S73.
133. Chauhan A, Lofton H, Maloney E, Moore J, Fol M, Madiraju MV, Rajagopalan M. 2006. Interference of Mycobacterium tuberculosis cell division by Rv2719c, a cell wall hydrolase. Mol Microbiol 62:132-147.
134. Plocinski P, Ziolkiewicz M, Kiran M, Vadrevu SI, Nguyen HB, Hugonnet J, Veckerle C, Arthur M, Dziadek J, Cross TA, Madiraju M, Rajagopalan M. 2011. Characterization of CrgA, a new partner of the Mycobacterium tuberculosis peptidoglycan polymerization complexes. J Bacteriol 193:3246-3256.
135. Plocinski P, Arora N, Sarva K, Blaszczyk E, Qin H, Das N, Plocinska R, Ziolkiewicz M, Dziadek J, Kiran M, Gorla P, Cross TA, Madiraju M, Rajagopalan M. 2012. Mycobacterium tuberculosis CwsA interacts with CrgA and Wag31, and the CrgA-CwsA complex is involved in peptidoglycan synthesis and cell shape determination. J Bacteriol 194:6398-6409.
136. Vadrevu IS, Lofton H, Sarva K, Blasczyk E, Plocinska R, Chinnaswamy J, Madiraju M, Rajagopalan M. 2011. ChiZ levels modulate cell division process in mycobacteria. Tuberculosis 91(Suppl 1): S128-S135.
137. England K, Crew R, Slayden RA. 2011. Mycobacterium tuberculosis septum site determining protein, Ssd encoded by rv3660c, promotes filamentation and elicits an alternative metabolic and dormancy stress response. BMC Microbiol 11:79.
138. Griffith DE, Aksamit TR. 2012. Therapy of refractory nontuberculous mycobacterial lung disease. Curr Opin Infect Dis 25: 218-227.
139. LiXZ, Zhang L, NikaidoH. 2004. Efflux pump-mediated intrinsic drug resistance in Mycobacterium smegmatis. Antimicrob Agents Chemother 48:2415-2423.
140. Chambers HF, Moreau D, Yajko D, Miick C, Wagner C, Hackbarth C, Kocagoz S, Rosenberg E, Hadley WK, Nikaido H. 1995. Can penicillins and other beta-lactam antibiotics be used to treat tuberculosis? Antimicrob Agents Chemother 39:2620-2624.
141. Cynamon MH, Palmer GS. 1983. In vitro activity of amoxicillin in combination with clavulanic acid against Mycobacterium tuberculosis. Antimicrob Agents Chemother 24:429-431.
142. Hugonnet JE, Tremblay LW, Boshoff HI, Barry CE 3rd, Blanchard JS. 2009. Meropenem-clavulanate is effective against extensively drugresistant Mycobacterium tuberculosis. Science 323:1215-1218.
143. Segura C, Salvado M, Collado I, Chaves J, Coira A. 1998. Contribution of beta-lactamases to beta-lactam susceptibilities of susceptible and multidrug-resistant Mycobacterium tuberculosis clinical isolates. Antimicrob Agents Chemother 42:1524-1526.
144. Sorg TB, Cynamon MH. 1987. Comparison of four beta-lactamase inhibitors in combination with ampicillin against Mycobacterium tuberculosis. J Antimicrob Chemother 19:59-64.
145. Wong CS, Palmer GS, Cynamon MH. 1988. In-vitro susceptibility of Mycobacterium tuberculosis, Mycobacterium bovis and Mycobacterium kansasii to amoxycillin and ticarcillin in combination with clavulanic acid. J Antimicrob Chemother 22:863-866.
146. Voladri RK, Lakey DL, Hennigan SH, Menzies BE, Edwards KM, Kernodle DS. 1998. Recombinant expression and characterization of the major beta-lactamase of Mycobacterium tuberculosis. Antimicrob Agents Chemother 42:1375-1381.
147. Hugonnet JE, Blanchard JS. 2007. Irreversible inhibition of the Mycobacterium tuberculosis beta-lactamase by clavulanate. Biochemistry 46:11998-12004.
148. Flores AR, Parsons LM, Pavelka MS Jr. 2005. Genetic analysis of the beta-lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to beta-lactam antibiotics. Microbiology 151:521-532.
149. Sala C, Haouz A, Saul FA, Miras I, Rosenkrands I, Alzari PM, Cole ST. 2009. Genome-wide regulon and crystal structure of BlaI (Rv1846c) from Mycobacterium tuberculosis. Mol Microbiol 71:1102-1116.
150. Nampoothiri KM, Rubex R, Patel AK, Narayanan SS, Krishna S, Das SM, Pandey A. 2008. Molecular cloning, overexpression and biochemical characterization of hypothetical beta-lactamases of Mycobacterium tuberculosis H37Rv. J Appl Microbiol 105:59-67.
151. Galleni M, Raquet X, Lamotte-Brasseur J, Fonze E, Amicosante G, Frere JM. 1995. DD-peptidases and beta-lactamases: catalytic mechanisms and specificities. J Chemother 7:3-7.
152. Rengarajan J, Bloom BR, Rubin EJ. 2005. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci USA 102:8327-8332.
153. Rengarajan J, Murphy E, Park A, Krone CL, Hett EC, Bloom BR, Glimcher LH, Rubin EJ. 2008. Mycobacterium tuberculosis Rv2224c modulates innate immune responses. Proc Natl Acad Sci USA 105: 264-269.
154. Deshayes C, Bach H, Euphrasie D, Attarian R, Coureuil M, Sougakoff W, Laval F, Av-Gay Y, Daffe M, Etienne G, Reyrat JM. 2010. MmpS4 promotes glycopeptidolipids biosynthesis and export in Mycobacterium smegmatis. Mol Microbiol 78:989-1003.
155. Daffé M, Crick DC, Jackson M. 2014. Genetics of capsular polysaccharides and cell envelope (glyco)lipids. Microbiol Spectrum 2(4): MGM2-0021-2013.