1887

3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of

Authors: Dean C. Crick1, Patrick J. Brennan2
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523; 2: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523
Content Type: Monograph
Publication Year: 2008
MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815783/9781555814687_Chap03-1.gif /docserver/preview/fulltext/10.1128/9781555815783/9781555814687_Chap03-2.gif

Abstract:

Recent developments in genomics, bioinformatics, proteomics, and analytical techniques have resulted in a more detailed and thorough understanding of the structure of the mycobacterial cell wall core and its biosynthesis. Indeed, much of the current interest in its biosynthesis is driven by the need for novel, alternative drugs to counteract drug-resistant tuberculosis. The tetrapeptide side chains of peptidoglycan (PG) consist of L-alanyl-D-isoglutaminylmeso-diaminopimelyl-D-alanine (L-Ala-D-Glu-Apm- D-Ala), with the Glu and Apm being further amidated. Recent mass spectrometric analysis suggests that the arabinan chains released from the cell wall by an endogenous arabinase are also approximately 30 residues long and indicates that galactosamine (GalNH) residues in Arabinogalactan (AG) isolated from the CSU20 strain are found on the C2 position of some of the internal 3,5-branched residues. Many of the insights to understanding the biosynthesis of the cell wall core are derived from earlier structural analysis. In general, polyprenyl diphosphate (Pol-P-P) molecules are synthesized through sequential condensation of isopentenyl diphosphate (IPP, derived from methylerythritol phosphate in mycobacteria) with allylic diphosphates, reactions that are catalyzed by prenyl diphosphate synthases. Synthesis of AG begins with the formation of the linker unit, and then there appears to be a concomitant extension of the galactan and arabinan moieties. The structural complexity of mycobacterial arabinofuran present in AG is likely to be reflected in a complex biosynthetic pathway, and arabinosyl transferases are now being rapidly identified in spp.

Citation: C. Crick D, J. Brennan P. 2008. 3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of , p 25-39. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch3

Key Concept Ranking

Bacterial Cell Wall
0.54214054
Cell Wall Biosynthesis
0.4637723
0.54214054
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of Mycobacterium tuberculosis
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815783.ch03-1,webId=/content/author/10.1128/9781555815783.ch03-1,properties={foaf_givenname=Dean, foaf_name=Dean C. Crick, foaf_surname=C. Crick, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815783.ch03-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815783.ch03-2,webId=/content/author/10.1128/9781555815783.ch03-2,properties={foaf_givenname=Patrick, foaf_name=Patrick J. Brennan, foaf_surname=J. Brennan, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815783.ch03-aff2]]}]]
Citation: C. Crick D, J. Brennan P. 2008. 3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of , p 25-39. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch3
/content/10.1128/9781555815783.ch03.ch03fig01
Figure 1.
Schematic diagram of the mycolyl-arabinogalactan-peptidoglycan complex of . The positions of the succinyl and -galactosamine residues are indicated ( ).
10.1128/9781555815783/f0026-01_thmb.gif
10.1128/9781555815783/f0026-01.gif
Image of Figure 1.
Figure 1.

Schematic diagram of the mycolyl-arabinogalactan-peptidoglycan complex of . The positions of the succinyl and -galactosamine residues are indicated ( ).

Citation: C. Crick D, J. Brennan P. 2008. 3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of , p 25-39. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch3
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555815783.ch03.ch03fig02
Figure 2.
Schematic diagram showing key intermediates in mycolyl-arabinogalactan-peptidoglycan complex synthesis and the central role played by decaprenyl phosphate.
10.1128/9781555815783/f0028-01_thmb.gif
10.1128/9781555815783/f0028-01.gif
Image of Figure 2.
Figure 2.

Schematic diagram showing key intermediates in mycolyl-arabinogalactan-peptidoglycan complex synthesis and the central role played by decaprenyl phosphate.

Citation: C. Crick D, J. Brennan P. 2008. 3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of , p 25-39. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch3
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555815783.ch03.ch03fig03
Figure 3.
Pathways involved in the biosynthesis of decaprenyl phosphate and peptidoglycan with respect to the topology of the plasma membrane. A simple hypothetical scheme for decaprenyl phosphate recycling has been included; more complex possibilities exist, as is discussed in the text. Gene (Rv) numbers have been provided for enzymes from which have been biochemically demonstrated to catalyze the indicated reaction. Symbols used: , phosphate; , -acylmuramic acid; , -acetylglucosamine.
10.1128/9781555815783/f0029-01_thmb.gif
10.1128/9781555815783/f0029-01.gif
Image of Figure 3.
Figure 3.

Pathways involved in the biosynthesis of decaprenyl phosphate and peptidoglycan with respect to the topology of the plasma membrane. A simple hypothetical scheme for decaprenyl phosphate recycling has been included; more complex possibilities exist, as is discussed in the text. Gene (Rv) numbers have been provided for enzymes from which have been biochemically demonstrated to catalyze the indicated reaction. Symbols used: , phosphate; , -acylmuramic acid; , -acetylglucosamine.

Citation: C. Crick D, J. Brennan P. 2008. 3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of , p 25-39. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch3
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555815783.ch03.ch03fig04
Figure 4.
Pathways involved in arabinogalactan synthesis showing the intersection of galactan synthesis and decaprenylphosphorylarabinose (DPA) synthesis. Gene (Rv) numbers have been provided for enzymes from which have been biochemically demonstrated to catalyze the indicated reaction ( ).
10.1128/9781555815783/f0030-01_thmb.gif
10.1128/9781555815783/f0030-01.gif
Image of Figure 4.
Figure 4.

Pathways involved in arabinogalactan synthesis showing the intersection of galactan synthesis and decaprenylphosphorylarabinose (DPA) synthesis. Gene (Rv) numbers have been provided for enzymes from which have been biochemically demonstrated to catalyze the indicated reaction ( ).

Citation: C. Crick D, J. Brennan P. 2008. 3 Biosynthesis of the Arabinogalactan-Peptidoglycan Complex of , p 25-39. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch3
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555815783.ch03
1. Adam, A.,, J. F. Petit,, J. Wietzerbi-Falszpan,, P. Sinay,, D. W. Thomas, and, E. Lederer. 1969. Mass spectrometric identification of N-glycolylmuramic acid, a constituent of Mycobacterium smegmatis walls. FEBS Lett. 4: 87– 92.
2. Alderwick, L. J.,, E. Radmacher,, M. Seidel,, R. Gande,, P. G. Hitchen,, H. R. Morris,, A. Dell,, H. Sahm,, L. Eggeling, and, G. S. Besra. 2005. Deletion of Cg-emb in Corynebacterianeae leads to a novel truncated cell wall arabinogalactan, whereas inactivation of Cg-ubiA results in an arabinan-deficient mutant with a cell wall galactan core. J. Biol. Chem. 280: 32362– 32371.
3. Alderwick, L. J.,, M. Seidel,, H. Sahm,, G. S. Besra, and, L. Eggeling. 2006. Identification of a novel arabinofuranosyl transferase (AftA) involved in cell wall arabinan biosynthesis in Mycobacterium tuberculosis. J. Biol. Chem. 281: 15653– 15661.
4. Allen, C. M.,, M. V. Keenan, and, J. Sack. 1976. Lactobacillus plantarum undecaprenyl pyrophosphate synthetase: purification and reaction requirements. Arch. Biochem. Biophys. 175: 236– 248.
5. Anderson, L., and, F. M. Unger. 1983. Bacterial liposaccharides. In ACS Symposium Series 231. American Chemical Society, Washington, DC.
6. Anderson, R. G.,, H. Hussey, and, J. Baddiley. 1972. The mechanism of wall synthesis in bacteria. The organization of enzymes and isoprenoid phosphates in the membrane. Biochem. J. 127: 11– 25.
7. Anonymous. 1987. Prenol nomenclature. Recommendations 1986. IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN). Eur. J. Biochem. 167: 181– 184.
8. Apfel, C. M.,, B. Takacs,, M. Fountoulakis,, M. Stieger, and, W. Keck. 1999. Use of genomics to identify bacterial undecaprenyl pyrophosphate synthetase: cloning, expression, and characterization of the essential uppS gene. J. Bacteriol. 181: 483– 492.
9. Argyrou, A., and, J. S. Blanchard. 2004. Kinetic and chemical mechanism of Mycobacterium tuberculosis 1-deoxy- d-xylulose-5-phosphate isomeroreductase. Biochemistry 43: 4375– 4384.
10. Baba, T., and, C. M. Allen, Jr. 1978. Substrate specificity of undecaprenyl pyrophosphate synthetase from Lactobacillus plantarum. Biochemistry 17: 5598– 5604.
11. Baddiley, J. 1972. Teichoic acids in cell walls and membranes of bacteria. Essays Biochem. 8: 35– 77.
12. Bailey, A. M.,, S. Mahapatra,, P. J. Brennan, and, D. C. Crick. 2002. Identification, cloning, purification, and enzymatic characterization of Mycobacterium tuberculosis 1-deoxy- d-xylulose 5-phosphate synthase. Glycobiology 12: 813– 820.
13. Banerjee, D. K. 1989. Amphomycin inhibits mannosylphosphoryldolichol synthesis by forming a complex with dolichylmonophosphate. J. Biol. Chem. 264: 2024– 2028.
14. Basu, J.,, R. Chattopadhyay,, M. Kundu, and, P. Chakrabarti. 1992. Purification and partial characterization of a penicillin-binding protein from Mycobacterium smegmatis. J. Bacteriol. 174: 4829– 4832.
15. Baulard, A. R.,, G. S. Besra, and, P. J. Brennan. 1999. The cell-wall core of Mycobacterium: structure, biogenesis and genetics, p. 240–259. In C. Ratledge and, J. Dale (ed.), Mycobacteria: Molecular Biology and Virulence. Blackwell Science Ltd, London, United Kingdom.
16. Belanger, A. E.,, G. S. Besra,, M. E. Ford,, K. Mikusova,, J. T. Belisle,, P. J. Brennan, and, J. M. Inamine. 1996. The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol. Proc. Natl. Acad. Sci. USA 93: 11919– 11924.
17. Berg, S.,, J. Starbuck,, J. B. Torrelles,, V. D. Vissa,, D. C. Crick,, D. Chatterjee, and, P. J. Brennan. 2005. Roles of conserved proline and glycosyltransferase motifs of embC in biosynthesis of lipoarabinomannan. J. Biol. Chem. 280: 5651– 5663.
18. Besra, G. S., and, P. J. Brennan. 1997. The mycobacterial cell wall: biosynthesis of arabinogalactan and lipoarabinomannan. Biochem. Soc. Trans. 25: 845– 850.
19. Besra, G. S.,, K. H. Khoo,, M. R. McNeil,, A. Dell,, H. R. Morris, and, P. J. Brennan. 1995. A new interpretation of the structure of the mycolyl-arabinogalactan complex of Mycobacterium tuberculosis as revealed through characterization of oligoglycosylalditol fragments by fast-atom bombardment mass spectrometry and 1H nuclear magnetic resonance spectroscopy. Biochemistry 34: 4257– 4266.
20. Besra, G. S.,, T. Sievert,, R. E. Lee,, R. A. Slayden,, P. J. Brennan, and, K. Takayama. 1994. Identification of the apparent carrier in mycolic acid synthesis. Proc. Natl. Acad. Sci. USA 91: 12735– 12739.
21. Billman-Jacobe, H.,, R. E. Haites, and, R. L. Coppel. 1999. Characterization of a Mycobacterium smegmatis mutant lacking penicillin binding protein 1. Antimicrob. Agents Chemother. 43: 3011– 3013.
22. Brennan, P. J., and, H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64: 29– 63.
23. Chambers, H. F.,, D. Moreau,, D. Yajko,, C. Miick,, C. Wagner,, C. Hackbarth,, S. Kocagoz,, E. Rosenberg,, W. K. Hadley, and, H. Nikaido. 1995. Can penicillins and other beta-lactam antibiotics be used to treat tuberculosis? Antimicrob. Agents Chemother. 39: 2620– 2624.
24. Chopra, I.,, L. Hesse, and, A. J. O’Neill. 2002. Exploiting current understanding of antibiotic action for discovery of new drugs. J. Appl. Microbiol. 92: 4S– 15S.
25. Crick, D. C.,, S. Mahapatra, and, P. J. Brennan. 2001. Biosynthesis of the arabinogalactan-peptidoglycan complex of Mycobacterium tuberculosis. Glycobiology 11: 107R– 118R.
26. Crick, D. C.,, L. Quadri, and, P. J. Brennan. 2008. p. 1–20. In S. H. E. Kaufmann and, E. Rubin (ed.), Handbook of Tuberculosis: Molecular Biology and Biochemistry. Wiley-VCH, Weinheim, Germany.
27. Crick, D. C.,, M. C. Schulbach,, E. E. Zink,, M. Macchia,, S. Barontini,, G. S. Besra, and, P. J. Brennan. 2000. Polyprenyl phosphate biosynthesis in Mycobacterium tuberculosis and Mycobacterium smegmatis. J. Bacteriol. 182: 5771– 5778.
28. Daffe, M.,, P. J. Brennan, and, M. McNeil. 1990. Predominant structural features of the cell wall arabinogalactan of Mycobacterium tuberculosis as revealed through characterization of oligoglycosyl alditol fragments by gas chromatography/mass spectrometry and by 1H and 13C NMR analyses. J. Biol. Chem. 265: 6734– 6743.
29. Daffe, M.,, M. McNeil, and, P. J. Brennan. 1993. Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodococcus, and Nocardia spp. Carbohydr. Res. 249: 383– 398.
30. Dal Nogare, A. R.,, N. Dan, and, M. A. Lehrman. 1998. Conserved sequences in enzymes of the UDP-GlcNAc/MurNAc family are essential in hamster UDP-GlcNAc:dolichol-P GlcNAc-1-P transferase. Glycobiology 8: 625– 632.
31. Dasgupta, A.,, P. Datta,, M. Kundu, and, J. Basu. 2006. The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 152: 493– 504.
32. De Smet, K. A.,, K. E. Kempsell,, A. Gallagher,, K. Duncan, and, D. B. Young. 1999. Alteration of a single amino acid residue reverses fosfomycin resistance of recombinant MurA from Mycobacterium tuberculosis. Microbiology 145: 3177– 3184.
33. Dhiman, R. K.,, M. L. Schaeffer,, A. M. Bailey,, C. A. Testa,, H. Scherman, and, D. C. Crick. 2005. 1-Deoxy-D-xylulose 5-phosphate reductoisomerase (IspC) from Mycobacterium tuberculosis: towards understanding mycobacterial resistance to fosmidomycin. J. Bacteriol. 187: 8395– 8402.
34. Dmitriev, B. A.,, S. Ehlers, and, E. T. Rietschel. 1999. Layered murein revisited: a fundamentally new concept of bacterial cell wall structure, biogenesis and function. Med. Microbiol. Immunol. (Berlin) 187: 173– 181.
35. Dmitriev, B. A.,, S. Ehlers,, E. T. Rietschel, and, P. J. Brennan. 2000. Molecular mechanics of the mycobacterial cell wall: From horizontal layers to vertical scaffolds. Int. J. Med. Microbiol. 290: 251– 258.
36. Dover, L. G.,, A. M. Cerdeno-Tarraga,, M. J. Pallen,, J. Parkhill, and, G. S. Besra. 2004. Comparative cell wall core biosynthesis in the mycolated pathogens, Mycobacterium tuberculosis and Corynebacterium diphtheriae. FEMS Microbiol. Rev. 28: 225– 250.
37. Draper, P. 1998. The outer parts of the mycobacterial envelope as permeability barriers. Front. Biosci. 3: D1253– D1261.
38. Draper, P.,, O. Kandler, and, A. Darbre. 1987. Peptidoglycan and arabinogalactan of Mycobacterium leprae. J. Gen. Microbiol. 133: 1187– 1194.
39. Draper, P.,, K. H. Khoo,, D. Chatterjee,, A. Dell, and, H. R. Morris. 1997. Galactosamine in walls of slow-growing mycobacteria. Biochem. J. 327: 519– 525.
40. El Ghachi, M.,, A. Bouhss,, D. Blanot, and, D. Mengin-Lecreulx. 2004. The bacA gene of Escherichia coli encodes a undecaprenyl pyrophosphate phosphatase activity. J. Biol. Chem. 279: 30106– 30113
41. El Ghachi, M.,, A. Derbise,, A. Bouhss, and, D. Mengin-Lecreulx. 2005. Identification of multiple genes encoding membrane proteins with undecaprenyl pyrophosphate phosphatase (UppP) activity in Escherichia coli. J. Biol. Chem. 280: 18689– 18695.
42. El Zoeiby, A.,, F. Sanschagrin, and, R. C. Levesque. 2003. Structure and function of the Mur enzymes: development of novel inhibitors. Mol. Microbiol. 47: 1– 12.
43. Escuyer, V. E.,, M. A. Lety,, J. B. Torrelles,, K. H. Khoo,, J. B. Tang,, C. D. Rithner,, C. Frehel,, M. R. McNeil,, P. J. Brennan, and, D. Chatterjee. 2001. The role of the embA and embB gene products in the biosynthesis of the terminal hexaarabinofuranosyl motif of Mycobacterium smegmatis arabinogalactan. J. Biol. Chem. 276: 48854– 48862.
44. Essers, L., and, H. J. Schoop. 1978. Evidence for incorporation of molecular oxygen, a pathway in biosynthesis of N-glycolylmuramic acid in Mycobacterium phlei. Biochim. Biophys. Acta 544: 180– 184.
45. Fujihashi, M.,, N. Shimizu,, Y. W. Zhang,, T. Koyama, and, K. Miki. 1999. Crystallization and preliminary X-ray diffraction studies of undecaprenyl diphosphate synthase from Micrococcus luteus B-P 26. Acta Crystallogr. D. 55: 1606– 1607.
46. Gateau, O.,, C. Bordet, and, G. Michel. 1976. Study of formation of N-glycolylmuramic acid from Nocardia asteroides. Biochim. Biophys. Acta 421: 395– 405.
47. Ghuysen, J. M. 1968. Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol. Rev. 32: 425– 464.
48. Ghuysen, J. M. 1991. Serine beta-lactamases and penicillin-binding proteins. Annu. Rev. Microbiol. 45: 37– 67.
49. Goffin, C., and, J. M. Ghuysen. 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.
50. Green, D. W. 2002. The bacterial cell wall as a source of antibacterial targets. Expert. Opin. Ther. Targets 6: 1– 19.
51. Hancock, I. C.,, S. Carman,, G. S. Besra,, P. J. Brennan, and, E. Waite. 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.
52. Higashi, Y.,, G. Siewert, and, J. L. Strominger. 1970. Biosynthesis of the peptidoglycan of bacterial cell walls. XIX. Isoprenoid alcohol phosphokinase. J. Biol. Chem. 245: 3683– 3690.
53. Higashi, Y., and, J. L. Strominger. 1970. Biosynthesis of the peptidoglycan of bacterial cell walls. XX. Identification of phosphatidylglycerol and cardiolipin as cofactors for isoprenoid alcohol phosphokinase. J. Biol. Chem. 245: 3691– 3696.
54. Higashi, Y.,, J. L. Strominger, and, C. C. Sweeley. 1967. Structure of a lipid intermediate in cell wall peptidoglycan synthesis: a derivative of a C 55 isoprenoid alcohol. Proc. Natl. Acad. Sci. USA 57: 1878– 1884.
55. Hoang, T. T.,, Y. Ma,, R. J. Stern,, M. R. McNeil, and, H. P. Schweizer. 1999. Construction and use of low-copy number T7 expression vectors for purification of problem proteins: purification of Mycobacterium tuberculosis RmlD and Pseudomonas aeruginosa LasI and Rh1I proteins, and functional analysis of purified Rh1I. Gene 237: 361– 371.
56. Huang, H. R.,, M. S. Scherman,, W. D’Haeze,, D. Vereecke,, M. Holsters,, D. C. Crick, and, M. R. McNeil. 2005. Identification and active expression of the Mycobacterium tuberculosis gene encoding 5-phospho-alpha- d-ribose-1-diphosphate: decaprenyl-phosphate 5-phosphoribosyltransferase, the first enzyme committed to decaprenylphosphoryl- d-arabinose synthesis. J. Biol. Chem. 280: 24539– 24543.
57. Jacobs, C.,, B. Joris,, M. Jamin,, K. Klarsov,, J. Vanbeeumen,, D. MenginLecreulx,, J. vanHeijenoort,, J. T. Park,, S. Normark, and, J. M. Frere. 1995. AmpD, essential for both beta-lactamase regulation and cell-wall recycling, is a novel cytosolic N-acetylmuramyl- l-alanine amidase. Mol. Microbiol. 15: 553– 559.
58. Jarlier, V.,, L. Gutmann, and, H. Nikaido. 1991. Interplay of cell-wall barrier and beta-lactamase activity determines high-resistance to beta-lactam antibiotics in Mycobacterium chelonae. Antimicrob. Agents Chemother. 35: 1937– 1939.
59. Jarlier, V., and, H. Nikaido. 1994. Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol. Lett. 123: 11– 18.
60. Kahan, F. M.,, J. S. Kahan,, P. J. Cassidy, and, H. Kropp. 1974. Mechanism of action of fosfomycin (phosphonomycin). Ann. N. Y. Acad. Sci. 235: 364– 386.
61. Kalin, J. R., and, C. M. Allen. 1979. Characterization of undecaprenol kinase from Lactobacillus plantarum. Biochim. Biophys. Acta 574: 112– 122.
62. Kalin, J. R., and, C. M. Allen. 1980. Lipid activation of undecaprenol kinase from Lactobacillus plantarum. Biochim. Biophys. Acta 619: 76– 89.
63. Kaur, D.,, P. J. Brennan, and, D. C. Crick. 2004. Decaprenyl diphosphate synthesis in Mycobacterium tuberculosis. J. Bacteriol. 186: 7564– 7570.
64. Keer, J.,, M. J. Smeulders,, K. M. Gray, and, H. D. Williams. 2000. Mutants of Mycobacterium smegmatis impaired in stationary-phase survival. Microbiology 146: 2209– 2217.
65. Khasnobis, S.,, J. Zhang,, S. K. Angala,, A. G. Amin,, M. R. McNeil,, D. C. Crick, and, D. Chatterjee. 2006. Characterization of a specific arabinosyltransferase activity involved in mycobacterial arabinan biosynthesis. Chem. Biol. 13: 787– 795.
66. Klutts, J. S.,, K. Hatanaka,, Y. T. Pan, and, A. D. Elbein. 2002. Biosynthesis of d-arabinose in Mycobacterium smegmatis: specific labeling from d-glucose. Arch. Biochem. Biophys. 398: 229– 239.
67. Kotani, S.,, I. Yanagida,, K. Kato, and, T. Matsuda. 1970. Studies on peptides, glycopeptides and antigenic polysaccharide-glycopeptide complexes isolated from an L-11 enzyme lysate of the cell walls of Mycobacterium tuberculosis strain H37Rv. Biken J. 13: 249– 275.
68. Kremer, L.,, L. G. Dover,, C. Morehouse,, P. Hitchin,, M. Everett,, H. R. Morris,, A. Dell,, P. J. Brennan,, M. R. McNeil,, C. Flaherty,, K. Duncan, and, G. S. Besra. 2001. Galactan biosynthesis in Mycobacterium tuberculosis: Identification of a bifunctional UDPgalactofuranosyltransferase. J. Biol. Chem. 276: 26430– 26440.
69. Lederer, E. 1971. The mycobacterial cell wall. Pure Appl. Chem. 25: 135– 165.
70. Lederer, E.,, A. Adam,, R. Ciorbaru,, J. F. Petit, and, J. Wietzerbin. 1975. Cell walls of mycobacteria and related organisms; chemistry and immunostimulant properties. Mol. Cell Biochem. 7: 87– 104.
71. Lee, R. E.,, P. J. Brennan, and, G. S. Besra. 1996. Mycobacterium tuberculosis cell envelope. Curr. Top. Microbiol. Immunol. 215: 1– 27.
72. Leyh-Bouille, M.,, R. Bonaly,, J. M. Ghuysen,, R. Tinelli, and, D. Tipper. 1970. LL-Diaminopimelic acid containing peptidoglycans in walls of Streptomyces spp. and of Clostridium perfringens (type-A). Biochemistry 9: 2944– 2952.
73. Liu, J.,, C. E. Barry, III,, G. S. Besra, and, H. Nikaido. 1996. Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J. Biol. Chem. 271: 29545– 29551.
74. Ma, Y.,, J. A. Mills,, J. T. Belisle,, V. Vissa,, M. Howell,, K. Bowlin,, M. S. Scherman, and, M. McNeil. 1997. Determination of the pathway for rhamnose biosynthesis in mycobacteria: cloning, sequencing and expression of the Mycobacterium tuberculosis gene encoding alpha- d-glucose-1-phosphate thymidylyltransferase. Microbiology 143: 937– 945.
75. Ma, Y.,, R. J. Stern,, M. S. Scherman,, V. D. Vissa,, W. Yan,, V. C. Jones,, F. Zhang,, S. G. Franzblau,, W. H. Lewis, and, M. R. McNeil. 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.
76. Mahapatra, S.,, J. Basu,, P. J. Brennan, and, D. C. Crick. 2005a. Structure, biosynthesis and genetics of the mycolic acid-arabinogalactan-peptidoglycan complex, p. 275–285. In S. T. Cole,, K. D. Eisenach,, D. N. McMurray, and, W. R. Jacobs (ed.), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC.
77. Mahapatra, S.,, D. C. Crick, and, P. J. Brennan. 2000. Comparison of the UDP- N-acetylmuramate: l-alanine ligase enzymes from Mycobacterium tuberculosis and Mycobacterium leprae. J. Bacteriol. 182: 6827– 6830.
78. Mahapatra, S.,, H. Scherman,, P. J. Brennan, and, D. C. Crick. 2005b. N-glycolylation of the nucleotide precursors of peptidoglycan biosynthesis of Mycobacterium spp. is altered by drug treatment. J. Bacteriol. 187: 2341– 2347.
79. Mahapatra, S.,, T. Yagi,, J. T. Belisle,, B. J. Espinosa,, P. J. Hill,, M. R. McNeil,, P. J. Brennan, and, D. C. Crick. 2005c. Mycobacterial lipid II is composed of a complex mixture of modified muramyl and peptide moieties linked to decaprenyl phosphate. J. Bacteriol. 187: 2747– 2757.
80. Marquardt, J. L.,, E. D. Brown,, W. S. Lane,, T. M. Haley,, Y. Ichikawa,, C. H. Wong, and, C. T. Walsh. 1994. Kinetics, stoichiometry, and identification of the reactive thiolate in the inactivation of UDP-GlcNAc enolpyruvoyl transferase by the antibiotic fosfomycin. Biochemistry 33: 10646– 10651.
81. Matsuhashi, M. 1966. Biosynthesis in the bacterial cell wall. Tanpakushitsu Kakusan Koso 11: 875– 886.
82. McNeil, M. 1999. Arabinogalactan in mycobacteria: structure, biosynthesis, and genetics, p. 207–223. In J. B. Goldberg (ed.), Genetics of Bacterial Polysaccharides. CRC Press, Washington, DC.
83. McNeil, M.,, G. S. Besra, and, P. J. Brennan. 1996. Chemistry of the mycobacterial cell wall, p. 171–185. In W. N. Rom and, S. M. Garay (ed.), Tuberculosis. Little, Brown and Company, Boston.
84. McNeil, M.,, M. Daffe, and, P. J. Brennan. 1991. Location of the mycolyl ester substituents in the cell walls of mycobacteria. J. Biol. Chem. 266: 13217– 13223.
85. McNeil, M. R., and, P. J. Brennan. 1991. Structure, function and biogenesis of the cell envelope of mycobacteria in relation to bacterial physiology, pathogenesis and drug resistance; some thoughts and possibilities arising from recent structural information. Res. Microbiol. 142: 451– 463.
86. Mengin-Lecreulx, D.,, J. vanHeijenoort, and, J. T. Park. 1996. Identification of the mpl gene encoding UDP-N-acetylmuramate: l-alanyl-gamma- d-glutamyl-meso-diaminopimelate ligase in Escherichia coli and its role in recycling of cell wall peptidoglycan. J. Bacteriol. 178: 5347– 5352.
87. Meroueh, S. O.,, K. Z. Bencze,, D. Hesek,, M. Lee,, J. F. Fisher,, T. L. Stemmler, and, S. Mobashery. 2006. Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc. Natl. Acad. Sci. USA 103: 4404– 4409.
88. Mikusova, K.,, M. Belanova,, J. Kordulakova,, K. Honda,, M. R. McNeil,, S. Mahapatra,, D. C. Crick, and, P. J. Brennan. 2006. Identification of a novel galactosyl transferase involved in biosynthesis of the mycobacterial cell wall. J. Bacteriol. 188: 6592– 6598.
89. Mikusova, K.,, H. R. Huang,, T. Yagi,, M. Holsters,, D. Vereecke,, W. D’Haeze,, M. S. Scherman,, P. J. Brennan,, M. R. McNeil, and, D. C. Crick. 2005. Decaprenylphosphoryl arabinofuranose, the donor of the D-arabinofuranosyl residues of mycobacterial arabinan, is formed via a two-step epimerization of decaprenylphosphoryl ribose. J. Bacteriol. 187: 8020– 8025.
90. Mikusova, K.,, M. Mikus,, G. S. Besra,, I. Hancock, and, P. J. Brennan. 1996. Biosynthesis of the linkage region of the mycobacterial cell wall. J. Biol. Chem. 271: 7820– 7828.
91. Mikusova, K.,, T. Yagi,, R. Stern,, M. R. McNeil,, G. S. Besra,, D. C. Crick, and, P. J. Brennan. 2000. Biosynthesis of the galactan component of the mycobacterial cell wall. J. Biol. Chem. 275: 33890– 33897.
92. Mills, J. A.,, K. Motichka,, M. Jucker,, H. P. Wu,, B. C. Uhlik,, R. J. Stern,, M. S. Scherman,, V. D. Vissa,, F. Pan,, M. Kundu,, Y. F. Ma, and, M. McNeil. 2004. Inactivation of the mycobacterial rhamnosyltransferase, which is needed for the formation of the arabinogalactan-peptidoglycan linker, leads to irreversible loss of viability. J. Biol. Chem. 279: 43540– 43546.
93. Minnikin, D. E. 1982. Lipids: complex lipids, their chemistry biosynthesis and roles, p. 95–184. In C. Ratledge and, J. Stanford (ed.), The Biology of Mycobacteria. Academic Press, London, United Kingdom.
94. Muth, J. D., and, C. M. Allen. 1984. Undecaprenyl pyrophosphate synthetase from Lactobacillus plantarum: a dimeric protein. Arch. Biochem. Biophys. 230: 49– 60.
95. Nikaido, H., and, V. Jarlier. 1991. Permeability of the mycobacterial cell-wall. Res. Microbiol. 142: 437– 443.
96. Park, J. T. 2001. Identification of a dedicated recycling pathway for anhydro- N-acetylmuramic acid and N-acetylglucosamine derived from Escherichia coli cell wall murein. J. Bacteriol. 183: 3842– 3847.
97. Petit, J. F.,, A. Adam, and, J. Wietzerbin-Falszpan. 1970. Constituents of Mycobacteria. 117. Isolation of UDP-N-Glycolylmuramyl (Ala, Glu, Dap) from Mycobacterium phlei. FEBS Lett. 6: 55– 57.
98. Petit, J. F.,, A. Adam,, J. Wietzerbin-Falszpan,, E. Lederer, and, J. M. Ghuysen. 1969. Chemical structure of the cell wall of Mycobacterium smegmatis. I. Isolation and partial characterization of the peptidoglycan. Biochem. Biophys. Res. Commun. 35: 478– 485.
99. Petit, J. F., and, E. Lederer. 1984. The structure of the mycobacterial cell wall, p. 301–322. In G. P. Kubica and, L. G. Wayne (ed.), The Mycobacteria, a Source Book. Marcel Dekker, New York, NY.
100. Raymond, J. B.,, S. Mahapatra,, D. C. Crick, and, M. S. Pavelka. 2005. Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J. Biol. Chem. 280: 326– 333.
101. Rieber, M.,, T. Imaeda, and, I. M. Cesari. 1969. Bacitracin action on membranes of mycobacteria. J. Gen. Microbiol. 55: 155– 159.
102. Rose, N. L.,, G. C. Completo,, S. J. Lin,, M. McNeil,, M. M. Palcic, and, T. L. Lowary. 2006. Expression, purification, and characterization of a galactofuranosyltransferase involved in Mycobacterium tuberculosis arabinogalactan biosynthesis. J. Am. Chem. Soc. 128: 6721– 6729.
103. Sassetti, C. M.,, D. H. Boyd, and, E. J. Rubin. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48: 77– 84.
104. Scherman, M.,, A. Weston,, K. Duncan,, A. Whittington,, R. Upton,, L. Deng,, R. Comber,, J. D. Friedrich, and, M. McNeil. 1995. Biosynthetic origin of mycobacterial cell wall arabinosyl residues. J. Bacteriol. 177: 7125– 7130.
105. Scherman, M. S.,, L. Kalbe-Bournonville,, D. Bush,, Y. Xin,, L. Deng, and, M. McNeil. 1996. Polyprenylphosphate-pentoses in mycobacteria are synthesized from 5-phosphoribose pyrophosphate. J. Biol. Chem. 271: 29652– 29658.
106. Schleifer, K. H., and, O. Kandler. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36: 407– 477.
107. Schulbach, M. C.,, P. J. Brennan, and, D. C. Crick. 2000. Identification of a short (C 15) chain Z-isoprenyl diphosphate synthase and a homologous long (C 50) chain isoprenyl diphosphate synthase in Mycobacterium tuberculosis. J. Biol. Chem. 275: 22876– 22881.
108. Schulbach, M. C.,, S. Mahapatra,, M. Macchia,, S. Barontini,, C. Papi,, F. Minutolo,, S. Bertini,, P. J. Brennan, and, D. C. Crick. 2001. Purification, enzymatic characterization, and inhibition of the Z-farnesyl diphosphate synthase from Mycobacterium tuberculosis. J. Biol. Chem. 276: 11624– 11630.
109. Seidel, M.,, L. J. Alderwick,, H. L. Birch,, H. Sahm,, L. Eggeling, and, G. S. Besra. 2007. Identification of a novel arabinofuranosyltransferase AftB involved in a terminal step of cell wall arabinan biosynthesis in Corynebacterianeae, such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J. Biol. Chem. 282: 14729– 14740.
110. Shimizu, N.,, T. Koyama, and, K. Ogura. 1998. Molecular cloning, expression, and characterization of the genes encoding the two essential protein components of Micrococcus luteus B-P 26 hexaprenyl diphosphate synthase. J. Bacteriol. 180: 1578– 1581.
111. Siewert, G., and, J. L. Strominger. 1967. Bacitracin—an inhibitor of dephosphorylation of lipid pyrophosphate an intermediate in biosynthesis of peptidoglycan of bacterial cell walls. Proc. Natl. Acad. Sci. USA 57: 767– 773.
112. Silver, L. L. 2003. Novel inhibitors of bacterial cell wall synthesis. Curr. Opin. Microbiol. 6: 431– 438.
113. Skarzynski, T.,, A. Mistry,, A. Wonacott,, S. E. Hutchinson,, V. A. Kelly, and, K. Duncan. 1996. Structure of UDP- N-acetylglucosamine enolpyruvyl transferase, an enzyme essential for the synthesis of bacterial peptidoglycan, complexed with substrate UDP- N-acetylglucosamine and the drug fosfomycin. Structure 4: 1465– 1474.
114. Stern, R. J.,, T. Y. Lee,, T. J. Lee,, W. Yan,, M. S. Scherman,, V. D. Vissa,, S. K. Kim,, B. L. Wanner, and, M. R. McNeil. 1999. Conversion of dTDP-4-keto-6-deoxyglucose to free dTDP-4-keto-rhamnose by the rmIC gene products of Escherichia coli and Mycobacterium tuberculosis. Microbiology 145: 663– 671.
115. Storm, D. R., and, J. L. Strominger. 1973. Complex formation between bacitracin peptides and isoprenyl pyrophosphates. The specificity of lipid-peptide interactions. J. Biol. Chem. 248: 3940– 3945.
116. Takayama, K.,, H. L. David,, L. Wang, and, D. S. Goldman. 1970a. Isolation and characterization of uridine diphosphate- N-glycolylmuramyl-L-alanyl-gamma- d-glutamyl-meso-alpha,alpha’-diaminopimelic acid from Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun. 39: 7– 12.
117. Takayama, K., and, D. S. Goldman. 1970b. Enzymatic synthesis of mannosyl-1-phosphoryl-decaprenol by a cell-free system of Mycobacterium tuberculosis. J. Biol. Chem. 245: 6251– 6257.
118. Takayama, K.,, H. K. Schnoes, and, E. J. Semmler. 1973. Characterization of the alkali-stable mannophospholipids of Mycobacterium smegmatis. Biochim. Biophys. Acta 316: 212– 221.
119. Takayama, K.,, C. Wang, and, G. S. Besra. 2005. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin. Microbiol. Rev. 18: 81– 101.
120. Templin, M. F.,, A. Ursinus, and, J. V. Holtje. 1999. A defect in cell wall recycling triggers autolysis during the stationary growth phase of Escherichia coli. EMBO J. 18: 4108– 4117.
121. Tripathi, R. P.,, N. Tewari,, N. Dwivedi, and, V. K. Tiwari. 2005. Fighting tuberculosis: An old disease with new challenges. Med. Res. Rev. 25: 93– 131.
122. van Heijenoort, J. 1994. Biosynthesis of bacterial peptidoglycan unit, p. 39–54. In J. M. Ghuysen and, R. Hakenbeck (ed.), Bacterial Cell Wall. Elsevier Medical Press, Amsterdam, The Netherlands.
123. van Heijenoort, J. 1996. Murein synthesis, p. 1025–1034. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, DC.
124. van Heijenoort, J. 1998. Assembly of the monomer unit of bacterial peptidoglycan. Cell. Mol. Life Sci. 54: 300– 304.
125. van Heijenoort, J. 2001a. Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11: 25R– 36R.
126. van Heijenoort, J. 2001b. Recent advances in the formation of the bacterial peptidoglycan monomer unit. Nat. Prod. Rep. 18: 503– 519.
127. Vilkas, E.,, C. Amar,, J. Markovits,, J. Vliegenthart, and, J. Kamerling. 1973. Occurrence of a galactofuranose disaccharide in immunoadjuvant fractions of Mycobacterium tuberculosis (cellwalls and wax D). Biochim. Biophys. Acta 297: 423– 435.
128. Vollmer, W., and, J. V. Holtje. 2004. The architecture of the murein (peptidoglycan) in gram-negative bacteria: Vertical scaffold or horizontal layer(s)? J. Bacteriol. 186: 5978– 5987.
129. Weston, A.,, R. J. Stern,, R. E. Lee,, P. M. Nassau,, D. Monsey,, S. L. Martin,, M. S. Scherman,, G. S. Besra,, K. Duncan, and, M. R. McNeil. 1997. Biosynthetic origin of mycobacterial cell wall galactofuranosyl residues. Tuber. Lung Dis. 78: 123– 131.
130. Wietzerbin, J.,, B. C. Das,, J. F. Petit,, E. Lederer,, M. Leyh-Bouille, and, J. M. Ghuysen. 1974. Occurrence of d-alanyl-(D)-mesodiaminopimelic acid and meso-diaminopimelyl-meso-diaminopimelic acid interpeptide linkages in the peptidoglycan of mycobacteria. Biochemistry 13: 3471– 3476.
131. Wietzerbin-Falszpan, J.,, B. C. Das,, I. Azuma,, A. Adam,, J. F. Petit, and, E. Lederer. 1970. Determination of amino acid sequences in peptides by mass spectrometry. 22. Isolation and mass spectrometric identification of peptide subunits of mycobacterial cell walls. Biochem. Biophys. Res. Commun. 40: 57– 63.
132. Willoughby, E.,, Y. Higashi, and, J. L. Strominger. 1972. Biosynthesis of peptidoglycan of bacterial cell-wall. 25. Enzymatic dephosphorylation of C55-isoprenylphosphate. J. Biol. Chem. 247: 5113– 5115.
133. Wolucka, B. A., and, E. de Hoffmann. 1995. The presence of beta-D-ribosyl-1-monophosphodecaprenol in mycobacteria. J. Biol. Chem. 270: 20151– 20155.
134. Wolucka, B. A., and, E. de Hoffmann. 1998. Isolation and characterization of the major form of polyprenyl-phospho-mannose from Mycobacterium smegmatis. Glycobiology 8: 955– 962.
135. Wolucka, B. A.,, M. R. McNeil,, E. de Hoffmann,, T. Chojnacki, and, P. J. Brennan. 1994. Recognition of the lipid intermediate for arabinogalactan/arabinomannan biosynthesis and its relation to the mode of action of ethambutol on mycobacteria. J. Biol. Chem. 269: 23328– 23335.
136. Wong, K. K., and, D. L. Pompliano. 1998. Peptidoglycan biosynthesis: unexploited targets within a familiar pathway, p. 197–217. In B. P. Rosen and, S. Mobashery (ed.), Resolving the Antibiotic Paradox. Kluwer Academic/Plenum Publishers, New York, NY.
137. Yagi, T.,, S. Mahapatra,, K. Mikusova,, D. C. Crick, and, P. J. Brennan. 2003. Polymerization of mycobacterial arabinogalactan and ligation to peptidoglycan. J. Biol. Chem. 278: 26497– 26504.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error