Arabinogalactan in mycobacteria: Structure, biosynthesis, and genetics

Genetics of Bacterial Polysaccharides

Volumn , Issue , 1999, Pages 207-223

  McNeil, Michael ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

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EID: 84861092845     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420074413     Document Type: Chapter

References (74)

1. McNeil, M. and P. J. Brennan. 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, pp. 451-463, 1991.
2. Brennan, P. J. and H. Nikaido. The envelope of mycobacteria. Annu. Rev. Biochem. 64, pp. 29-63, 1995.
3. Takayama, K. and J. O. Kilburn. Inhibition of synthesis of arabinogalactan by ethambutol in Mycobacterium smegmatis. Antimicrob. Agents Chemother. 33, pp. 1493-1499, 1989.
4. Deng, L., K. Mikusova, K. G. Robuck, M. Scherman, P. J. Brennan, and M. Mc-Neil. Recognition of multiple effects of ethambutol on the metabolism of the mycobacterial cell envelope. Antimicrob. Agents Chemother. 39, pp. 694-701, 1995.
5. Lee, Y. C. and C. E. Ballou. Complete structures of the glycophospholipids of mycobacteria. Biochemistry 4, pp. 1395-1404, 1965.
6. Khoo, K. H., A. Dell, H. R. Morris, P. J. Brennan, and D. Chatterjee. Structural definition of acylated phosphatidylinositol mannosides from Mycobacterium tuberculosis: definition of a common anchor for lipomannan and lipoarabinomannan. Glycobiology 5, pp. 117-127, 1995.
7. Hunter, S. W., H. Gaylord, and P. J. Brennan. Structure and antigenicity of the phosphorylated lipopolysaccharide antigens from the leprosy and tubercle bacilli. J. Biol. Chem. 261, pp. 12345-12351, 1986.
8. Khoo, K.H., A. Dell, H. R. Morris, P. J. Brennan, and A. K. Chatterjee. Inositol phosphate capping of the nonreducing termini of lipoarabinomannan from rapidly growing strains of Mycobacterium. J. Biol. Chem. 270, pp. 12380-12389, 1995.
9. Khoo, K. H., A. Dell, H. R. Morris, P. J. Brennan, and D. Chatterjee. Inositol phosphate capping of the nonreducing termini of lipoarabinomannan from rapidly growing strains of Mycobacterium. J. Biol. Chem. 270, pp. 12380-12389, 1995.
10. Chatterjee, D., K. H. Khoo, M. R. McNeil, A. Dell, H. R. Morris, and P. J. Brennan. Structural definition of the non-reducing termini of mannose-capped LAM from Mycobacterium tuberculosis through selective enzymatic degradation and fast atom bombardment-mass spectrometry. Glycobiology 3, pp. 497-506, 1993.
11. Chatterjee, D., S. W. Hunter, M. McNeil, and P. J. Brennan. Lipoarabinomannan: multiglycosylated form of the mycobacterial mannosylphosphatidylinositols. J. Biol. Chem. 267, pp. 6228-6233, 1992.
12. Aspinall, G. O., D. Chatterjee, and P. J. Brennan. The variable surface glycolipids of mycobacteria: structures, synthesis of epitopes, and biological properties. [Review]. Adv. Carbohydr. Chem. Biochem. 51, pp. 169-242, 1995.
13. McNeil, M., D. Chatterjee, S. W. Hunter, and P. J. Brennan. Mycobacterial glycolipids: isolation, structures, antigenicity, and synthesis of neoantigens, in Methods in Enzymology, Ginsburg V. (Ed.), Academic Press. San Diego. 1989.
14. Ortalo-Magne, A., M. A. Dupont, A. Lemassu, A. B. Andersen, P. Gounon, and M. Daffe. Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology 141, pp. 1609-1620, 1995.
15. Lemassu, A., A. Ortalo-Magne, F. Bardou, G. Silve, M. A. Laneelle, and M. Daffe. Extracellular and surface-exposed polysaccharides of non-tuberculous mycobacteria. Microbiology 142, pp. 1513-1520, 1996.
16. Lemassu, A. and M. Daffe. Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis. Biochem. J. 297, pp. t2)351-t2)357, 1994.
17. Cohen, M. L. Epidemiology of drug resistance: Implications for a post-antimicrobial era. Science 257, pp. 1050-1052, 1992.
18. Bloom, B. R. Foreword. Tuberculosis, First edition, Rom, W.N. and Garay, S. (Eds.), Little, Brown, Boston. 1996.
19. Moran, N. WHO issues another gloomy tuberculosis report. Nature Med. 2, p. 377, 1996.
20. McNeil, M. Targeted preclinical drug development for Mycobacterium avium complex: a biochemical approach, in Mycobacterium avium-Complex Infection, Korvick, J.A. and Benson, C.A. (Eds.), Marcel Dekker, New York. 1996.
21. Kaplan, G., R. R. Gandhi, D. E. Weinstein, W. R. Levis, M. E. Patarroyo, P. J. Brennan, and Z. A. Cohn. Mycobacterium leprae antigen-induced suppression of T cell proliferation in vitro. J. Immunol. 138, pp. 3028-3034, 1987.
22. Sibley, L. D., S. W. Hunter, P. J. Brennan, and J. L. Krahenbuhl. Mycobacterial lipoarabinomannan inhibits gamma interferon-mediated activation of macrophages. Infect. Immun. 56, pp. 1232-1236, 1988.
23. Chan, J., X. Fan, S. W. Hunter, P. J. Brennan, and B. R. Bloom. Lipoarabinomannan, a possible virulence factor involved in persistence of Mycobacterium tuberculosis within macrophages. Infect. Immun. 59, pp. 1755-1761, 1991.
24. Moreno, C., A. Mehlert, and J. Lamb. The inhibitory effects of mycobacterial lipoarabinomannan and polysaccharides upon polyclonal human T-cell proliferation. Clin. Exp. Immunol. 74, pp. 206-210, 1988.
25. Moreno, C., J. Taverne, A. Mehlert, C. A. W. Bate, R. J. Brealey, A. Meager, G. A. W. Rook, and J. H. L. Playfair. Lipoarabinomannan from Mycobacterium tuberculosis induces the production of tumor necrosis factor from human and murine macrophages. Clin. Exp. Immunol. 76, pp. 240-245, 1989.
26. Chatterjee, D., A. D. Roberts, K. Lowell, P. J. Brennan, and I. M. Orme. Structural basis of capacity of lipoarabinomannan to induce secretion of tumor necrosis factor. Infect. Immun. 60, pp. 1249-1253, 1992.
27. Adams, L. B., Y. Fukutomi, and J. L. Krahenbuhl. Regulation of murine macrophage effector functions by lipoarabinomannan from mycobacterial strains with different degrees of virulence. Infect. Immun. 61, pp. 4173-4181, 1993.
28. Barnes, P. F., D. Chatterjee, J. S. Abrams, S. Lu, E. Wang, M. Yamamura, P. J. Brennan, and R. L. Modlin. Cytokine production induced by Mycobacterium tuberculosis lipoarabinomannan: relationship to chemical structure. J. Immunol. 149, pp. 541-547, 1992.
29. Rastogi, N., K. S. Goh, and H. L. David. Enhancement of drug susceptibility of Mycobacterium avium by inhibitors of cell envelope synthesis. Antimicrob. Agents Chemother. 34, pp. 759-764, 1990.
30. Rastogi, N. Recent observations concerning structure and function relationships in the mycobacterial cell envelope: elaboration of a model in terms of mycobacterial pathogenicity, virulence and drug resistance. Res. Microbiol. 142, pp. 464-476, 1991.
31. Belisle, J. T., L. Pascopella, J. M. Inamine, P. J. Brennan, and W. R. Jacobs. Isolation and expression of a gene cluster responsible for the biosynthesis of the glycopeptidolipid antigens of Mycobacterium avium. J. Bacteriol. 173, pp. 6991-6997, 1991.
32. Belisle, J. T., K. Klaczkiewicz, P. J. Brennan, W. R. Jacobs, and J. M. Inamine. Rough morphological variants of Mycobacterium avium: characterization of genomic deletions resulting in the loss of glycopeptidolipid expression. J. Biol. Chem. 268, pp. 10517-10523, 1993.
33. Besra, G. S., C. B. Morehouse, C. M. Rittner, C. J. Waechter, and P. J. Brennan. Biosynthesis of mycobacterial lipoarabinomannan. J. Biol. Chem. 272, pp. 18460-18466, 1997.
34. Belisle, J. T., M. McNeil, D. Chatterjee, J. M. Inamine, and P. J. Brennan. Expression of the core lipopeptide of the glycopeptidolipid surface antigens in rough mutants of Mycobacterium avium. J. Biol. Chem. 268, pp. 10510-10516, 1993.
35. Mills, J. A., M. McNeil, J. T. Belisle, W. R. Jacobs, and P. J. Brennan. Genetic loci of Mycobacterium avium ser2 gene cluster and their functions. J. Bacteriol. 176, pp. 4803-4808, 1994.
36. Besra, G. S., K.H. Khoo, M. McNeil, A. Dell, H. R. Morris, and P. J. Brennan. 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, pp. 4257-4266, 1995.
37. McNeil, M., M. Daffe, and P. J. Brennan. Location of the mycolyl ester substituent in the cell walls of mycobacteria. J. Biol. Chem. 266, pp. 13217-13223, 1991.
38. Daffe, M., P. J. Brennan, and M. McNeil. 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, pp. 6734-6743, 1990.
39. McNeil, M., M. Daffe, and P. J. Brennan. Evidence for the nature of the link between the arabinogalactan and peptidoglycan components of mycobacterial cell walls. J. Biol. Chem. 265, pp. 18200-18206, 1990.
40. Besra, G. S. and P. J. Brennan. The mycobacterial cell envelope: a target for novel drugs against tuberculosis. J. Pharm. Pharmacol. 49, pp. 25-30, 1997.
41. Lee, R. E., K. Mikusova, P. J. Brennan, and G. S. Besra. Synthesis of the mycobacterial arabinose donor β-D-Arabinofuranosyl-1-monophosphoryldecaprenol, development of a basic arabinosyl-transferase assay and identification of ethambutol as an arabinosyl transferase inhibitor. J. Am. Chem. Soc. 117, pp. 11829-11832, 1995.
42. Mikusova, K., M. Mikus, G. Besra, I. Hancock, and P. J. Brennan. Biosynthesis of the linkage region of the mycobacterial cell wall. J. Biol. Chem. 271, pp. 7820-7828, 1996.
43. Xin, Y., R. E. Lee, M. S. Scherman, K. H. Khoo, G. S. Besra, P. J. Brennan, and M. McNeil. Characterization of the in vitro synthesized arabinan of mycobacterial cell walls. Biochim. Biophys. Acta 1335, pp. 231-234, 1997.
44. Ma, Y., J. A. Mills, J. T. Belisle, V. Vissa, M. Howell, K. Bowlin, M. S. Scherman, and M. McNeil. Determination of the pathway for rhamnose biosynthesis in mycobacteria: cloning, sequencing, and expression of the Mycobacterium tuberculosis gene encoding α-D-glucose-1-phosphate thymidylyltransferase. Microbiology 143, pp. 937-945, 1997.
45. Scherman, M. S., L. Kalbe-Bournonville, D. Bush, Y. Xin, and M. McNeil. Polyprenylphosphate-pentoses in mycobacteria are synthesized from phosphoribose pyrophosphate. J. Biol. Chem. 271, pp. 29652-29658, 1996.
46. Scherman, M., A. Weston, K. Duncan, A. Whittington, R. Upton, L. Deng, R. Comber, J. D. Friedrich, and M. McNeil. The biosynthetic origin of the mycobacterial cell wall arabinosyl residues. J. Bacteriol. 177, pp. 7125-7130, 1995.
47. Shibaev, V. N. Biosynthesis of bacterial polysaccharide chains composed of repeating units. [Review]. Adv. Carbohydr. Chem. Biochem. 44, pp. 277-339, 1986.
48. 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. The biosynthetic origin of the mycobacterial cell wall galactofuranosyl residues. Tubercle and Lung Disease 78, pp. 123-131, 1998.
49. Nassau, P. M., S. L. Martin, R. E. Brown, A. Weston, D. Monsey, M. McNeil, and K. Duncan. Galactofuranose Biosynthesis in Escherichia coli K12: Identification and cloning of UDP-galactopyranose mutase. J. Bacteriol. 178, pp. 1047-1052, 1996.
50. Lee, R., D. Monsey, A. Weston, K. Duncan, C. Rithner, and M. McNeil. Enzymatic synthesis UDP-galactofuranose and assays for UDP-galactopyranosyl mutase based on HPLC and on linked enzymatic production of NADH. Anal. Biochem. 242, pp. 1-7, 1996.
51. Wolucka, B. A., M. R. McNeil, E. de Hoffmann, T. Chojnacki, and P. J. Brennan. 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, pp. 23328-23335, 1994.
52. Reeves, P. R., M. Hobbs, M. A. Valvano, M. Skurnik, C. Whitfield, D. Coplin, N. Kido, J. Klena, D. Maskell, C. R. Raetz, and P. D. Rick. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol. 4, pp. 495-503, 1996.
53. Stevenson, G., B. Neal, D. Liu, M. Hobbs, N. H. Packer, M. Batley, J. W. Redmond, L. Lindquist, and P. R. Reeves. Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster. J. Bacteriol. 176, pp. 4144-4156, 1994.
54. Lee, T. Y., T. J. Lee, J. T. Belisle, P. J. Brennan, and S. K. Kim. A novel repeat sequence specific to Mycobacterium tuberculosis complex and its implications. Tubercle and Lung Disease 78, pp. 13-19, 1997.
55. Lee, T. Y., R. J. Stern, M. S. Scherman, and W. Yan. Unpublished data 1998.
56. Koplin, R., J. R. Brisson, and C. Whitfield. UDP-galactofuranose precursor required for formation of the lipopolysaccharide O antigen of Klebsiella pneumoniae serotype 1 is synthesized by the product of the rfbDKPO1 gene. J. Biol. Chem. 272, pp. 4121-4128, 1997.
57. Szumilo, T. The occurrence of the Leloir pathway in non-pathogenic mycobacteria. Acta Microbiol. Polonica 30, pp. 327-336, 1981.
58. Yokoyama, K. and C. E. Ballou. Synthesis of α-1-6-mannooligosaccharide in M. smegmatis. J. Biol. Chem. 264, pp. 21621-21628, 1989.
59. Schultz, J. and A. D. Elbein. Biosynthesis of mannosyl- and glucosyl-phosphoryl polyprenols in Mycobacterium smegmatis. Arch. Biochem. Biophys. 160, pp. 311-322, 1974.
60. Takayama, K. and D. S. Goldman. Enzymatic synthesis of mannosyl-1-phosphoryldecaprenol by a cell-free system of Mycobacterium tuberculosis. J. Biol. Chem. 245, pp. 6251-6257, 1970.
61. Singh, S. and S. E. Hogan. Isolation and characterization of sugar nucleotides from Mycobacterium smegmatis. Microbios. 77, pp. 217-222, 1994.
62. Mills, J. A. Unpublished data 1997.
63. Liu, D. and P. R. Reeves. Escherichia coli K12 regains its O antigen. Microbiology 140, pp. 49-57, 1994.
64. Mills, J. A., K. Motichka, R. J. Stern, M. S. Scherman, and M. R. McNeil. Manuscript in preparation 1999.
65. Besra, G. S. and P. J. Brennan. The mycobacterial cell wall: biosynthesis of arabinogalactan and lipoarabinomannan. Biochem. Soc. Trans. 25, pp. 845-850, 1997.
66. Lee, R. E., P. J. Brennan, and G. S. Besra. Mycobacterial arabinan biosynthesis: the use of synthetic arabinoside acceptors in the development of an arabinosyl transfer assay. Glycobiology 7, pp. 1121-1128, 1997.
67. Belanger, A. E., G. S. Besra, M. E. Ford, K. Mikusova, J. Belisle, P. J. Brennan, and J. M. Inamine. Molecular characterization of the target of the antimycobacterial drug ethambutol. Proc. Natl. Acad. Sci. U.S.A. 93, pp. 11919-11924, 1996.
68. Mikusova, K., R. A. Slayden, G. S. Besra, and P. J. Brennan. Biogenesis of the mycobacterial cell wall and the site of action of ethambutol. Antimicrob. Agents Chemother. 39, pp. 2484-2489, 1995.
69. Besra, G. S., T. Sievert, R. E. Lee, R. A. Slayden, P. J. Brennan, and K. Takayama. Identification of the apparent carrier in mycolic acid synthesis. Proc. Natl. Acad. Sci. U.S.A. 91, pp. 12735-12739, 1995.
70. Belisle, J. T., V. D. Vissa, T. Sievert, K. Takayama, P. J. Brennan, and G. S. Besra. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276, pp. 1420-1422, 1997.
71. Husson, R. N., B. E. James, and R. A. Young. Gene replacement and expression of foreign DNA in mycobacteria. J. Bacteriol. 172, pp. 519-524, 1990.
72. Sander, P., A. Meier, and E. C. Bottger. RspL+: A dominant selectable marker for gene replacement in mycobacteria. Mol. Microbiol. 16, pp. 991-1000, 1995.
73. Kalpana, G. V., B. R. Bloom, and W. R. Jacobs. Insertional mutagenesis and illegitimate recombination in mycobacteria. Proc. Natl. Acad. Sci. U.S.A. 88, pp. 5433-5437, 1991.
74. Parish, T. and N. G. Stoker. Development and use of a conditional antisense mutagenesis system in mycobacteria. FEMS Microbiol. Lett. 154, pp. 151-157, 1997.