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Chapter 17 : The Cell Envelope of Mycobacterium tuberculosis with Special Reference to the Capsule and Outer Permeability Barrier

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The Cell Envelope of Mycobacterium tuberculosis with Special Reference to the Capsule and Outer Permeability Barrier, Page 1 of 2

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Abstract:

This chapter concentrates on a few topics of current interest in the field of envelope studies, particularly the permeability of the cell envelope of . A good deal of research was done on the plasma membranes of rapidly growing mycobacteria, but rather little is known specifically about the membrane of . There is every reason to suppose that mycobacterial membranes are structurally and functionally very similar to other bacterial plasma membranes. Mycobacterial peptidoglycan belongs to a family of structures possessed by almost all eubacteria but by no other type of living organism. The recent discovery of the mixture of proteins and polysaccharides that accumulates around unstirred in vitro, and presumably around the bacterium as it grows within a vacuole in a cell of its human host, is unexpected. Extraction of the envelope of with solvents releases a bewildering variety of substances, especially lipids and glycolipids. Porin-like proteins have been identified in the envelope of the rapidly growing nonpathogen , and one of these has been sequenced. The investigation of mycobacterial porins, including those from , has already produced some exciting data, but our understanding is far from complete. , with its complex structure and metabolic capabilities and its ability to grow in several contrasting environments, is a fascinating subject for research.

Citation: Draper P, Daffé M. 2005. The Cell Envelope of Mycobacterium tuberculosis with Special Reference to the Capsule and Outer Permeability Barrier, p 261-274. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch17

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Bacterial Proteins
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Outer Membrane Proteins
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Gel Permeation Chromatography
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Figure 1

Envelope of . (A) Electron micrograph of ultrathin section of a strain of the complex. Photograph courtesy of J. L. Koeck, Laboratory of Electron Microscopy, HIA Val-de-Grace, France. (B) Diagram of the construction of the envelope (the layers are only roughly to scale). 1, position of superficial lipids of the capsule. 2, capsule mainly of polysaccharide and protein (the outer margin is ill defined unless the bacterium is within a phagocytic cell); 3, position of “buried” lipids in the capsule; 4, mycolate layer, probably including other lipids; 5, peptidoglycan plus arabinogalactan (arrangement not established); 6, triple-layer plasma membrane, with the outer layer being somewhat thicker (in electron micrographs) than the inner layer.

Citation: Draper P, Daffé M. 2005. The Cell Envelope of Mycobacterium tuberculosis with Special Reference to the Capsule and Outer Permeability Barrier, p 261-274. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch17
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Image of Figure 2
Figure 2

Permeability barriers of mycobacteria. The diagram shows the capsule, the outer permeability barrier comprising mycolates and other lipids, arabinogalactan (AG) plus peptidoglycan (PG), and the plasma membrane. The capsule and AG+PG are hydrophilic but are likely to impede the diffusion of large molecules. The outer permeability barrier and the plasma membrane allow the diffusion of lipophilic molecules. A porin is represented in the outer permeability barrier, and a transport protein is shown in the plasma membrane; these proteins allow the passage of hydrophilic molecules.

Citation: Draper P, Daffé M. 2005. The Cell Envelope of Mycobacterium tuberculosis with Special Reference to the Capsule and Outer Permeability Barrier, p 261-274. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch17
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References

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1. Adam, A.,, J. F. Petit,, J. Wietzerbin-Falszpan,, P. Sinay,, D. W. Thomas,, and E. Lederer. 1969. L’acide N-glycolyl-muramique, constituant des parois de Mycobacterium smegmatis: identification par spectrométrie de masse. FEBS Lett. 4:8792.
2. Aiba, H.,, F. Nakasai,, S. Mizushima,, and T. Mizuno. 1989. Evidence for the physiological importance of the phosphotransfer between the two regulatory components, EnvZ and OmpR, in osmoregulation in Escherichia coli. J. Biol. Chem. 264:1409014094.
3. Amar-Nacasch, C.,, and E. Vilkas. 1970. Étude des parois de Mycobacterium tuberculosis. II. Mise en évidence d’un mycolate d’arabinobiose et d’un glucane dans les parois de M. tuberculosis H37Ra. Bull. Soc. Chim. Biol. 52:145151.
4. Antoine, A. D.,, and B. S. Tepper. 1969. Characterization of glycogen from mycobacteria. Arch. Biochem. Biophys. 134: 207213.
5. Arora, A.,, D. Rinehart,, G. Szabo,, and L. K. Tamm. 2000. Refolded outer membrane protein A of Escherichia coli forms ion channels with two conductive states in planar lipid bilayers. J. Biol. Chem. 275:15941600.
6. Asselineau, C.,, J. Asselineau,, G. Lanéelle,, and M. A. Lanéelle. 2002. The biosynthesis of mycolic acids by mycobacteria: current and alternative hypotheses. Prog. Lipid Res. 41:501523.
7. Beatty, W. L.,, E. R. Rhoades,, H. J. Ullrich,, D. Chatterjee,, J. E. Heuser,, and D. G. Russell. 2000. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1:235247.
8. Beatty, W. L.,, and D. G. Russell. 2000. Identification of mycobacterial surface proteins released into subcellular compartments of infected macrophages. Infect. Immun. 68:69977002.
9. Beatty, W. L.,, H. J. Ullrich,, and D. G. Russell. 2001. Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event. Eur. J. Cell Biol. 80:3140.
10. Brennan, P. J.,, and H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64:2963.
11. Brinkman, F. S. L.,, M. Bains,, and R. E. W. Hancock. 2000. The amino terminus of Pseudomonas aeruginosa outer membrane protein OprF forms channels in lipid bilayers membranes: correlation with a three-dimensional model. J. Bacteriol. 182:52515255.
12. Brown, I. N.,, and P. Draper. 1976. Growth of Mycobacterium lepraemurium in the mouse bone marrow: an ultrastructural study. Infect. Immun. 13:11991204.
13. Chambers, H. F.,, D. Moreau,, D. Yaijko,, C. Miick,, C. Wagner,, C. Hackbarth,, S. Kocagöz,, and H. Nikaido. 1995. Can penicillins and other beta-lactam antibiotics be used to treat tuberculosis? Antimicrob. Agents Chemother. 39:26202624.
14. Cole, S. T.,, R. Brosch,, J. Parkhill,, T. Garnier,, C. Churcher,, D. Harris,, S. V. Gordon,, K. Eiglmeier,, S. Gas,, C. E. Barry III,, F. Tekaia,, K. Badcock,, D. Basham,, D. Brown,, T. Chillingworth,, R. Connor,, R. Davies,, K. Devlin,, T. Feltwell,, S. Gentles,, N. Hamlin,, S. Holroyd,, T. Hornsby,, K. Jagels,, A. Krogh,, J. McLean,, S. Moule,, L. Murphy,, K. Oliver,, J. Osborne,, M. A. Quail,, M.-A. Rajandream,, J. Rogers,, S. Rutter,, K. Seeger,, J. Skelton,, R. Squares,, S. Squares,, J. E. Sulston,, K. Taylor,, S. Whitehead,, and B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537544.
15. Daffé, M.,, and P. Draper. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39:131203.
16. Daffé, M.,, and G. Etienne. 1999. The capsule of Mycobacterium tuberculosis and its implications for pathogenicity. Tubercle Lung Dis. 79:153169.
17. Daffé, M.,, and A. Lemassu,. 2000. Glycomicrobiology of the mycobacterial cell surface: structure and biological activities of the cell envelope glycoconjugates, p. 225273. In R.J. Doyle (ed.), Glycomicrobiology. Kluwer Academic/Plenum Press, New York, N.Y.
18. Daffé, 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. 265:67346743.
19. Daffé, M.,, P. J. Brennan,, and M. McNeil. 1993. Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodococcus, and Nocardia spp. Carbohydr. Res. 249:383398.
20. Daniel, T. M., 1984. Soluble mycobacterial antigens, p. 417465. In G. P. Kubica, and L. G. Wayne (ed.), The Mycobacteria: a Sourcebook, part A. Marcel Dekker, Inc., New York, N.Y.
20a.. Dinadayala, P.,, A. Lemassu,, P. Granovski,, S. Cerantola,, N. Winter,, and M. Daffé. 2004. Revisiting the structure of the anti-neoplastic glucans of Mycobacterium bovis Bacille Calmette- Guerin. Structural analysis of the extracellular and boiling water extract-derived glucans of the vaccine substrains. J. Biol. Chem. 279:1236912378.
21. Draper, P. 1971. The walls of Mycobacterium lepraemurium: chemistry and ultrastructure. J. Gen. Microbiol. 69:313324.
22. Draper, P., 1982. The anatomy of mycobacteria, p. 952. In C. Ratledge, and J. Stanford (ed.), The Biology of the Mycobacteria, vol. 1. Physiology, Identification and Classification. Academic Press, Ltd., London, United Kingdom.
23. Draper, P. 1998. The outer parts of the mycobacterial envelope as permeability barriers. Front. Biosci. 3:12531261.
24. Draper, P.,, O. Kandler,, and A. Darbre. 1987. Peptidoglyacn and arabinogalactan of Mycobacterium leprae. J. Gen Microbiol. 133:11871194.
25. Draper, P.,, K. H. Khoo,, D. Chatterjee,, A. Dell,, and H. R. Morris. 1997. Galactosamine in walls of slow-growing mycobacteria. Biochem. J. 327:519525.
26. Dubnau, E.,, J. Chan,, C. Raynaud,, V. P. Mohan,, M. A. Lanéelle,, K. Yu,, A. Quémard,, I. Smith,, and M. Daffé. 2000. Oxygenated mycolic acids are necessary for virulence of M. tuberculosis in mice. Mol. Microbiol. 36:630637.
27. Engelhardt, H.,, C. Heinz,, and M. Niederweis. 2002. A tetrameric porin limits the cell wall permeability of Mycobacterium smegmatis. J. Biol. Chem. 277:3756737572.
27a.. Faller, M.,, M. Niederweis,, and G. E. Schulz. 2004. The structure of a mycobacterial outer-membrane channel. Science 303:11891192.
28. Fratti, R. A.,, J. Chua,, I. Vergne,, and V. Deretic. 2003. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100:54375442.
29. Heinz, C.,, H. Engelhardt,, and M. Niederweis. 2003. The core of the tetrameric mycobacterial porin MspP is an extremely stable β-sheet domain. J. Biol. Chem. 278:86788685.
30. Jackson, M.,, C. Raynaud,, M. A. Lanéelle,, C. Guilhot,, C. Laurent- Winter,, D. Ensergueix,, B. Gicquel,, and M. Daffé. 1999. Inactivation of the antigen 85C gene profoundly affects the mycolate content and alters the permeability of the Mycobacterium tuberculosis cell envelope. Mol. Microbiol. 31:15731587.
31. Jarlier, V.,, and H. Nikaido. 1990. Permeability barrier to hydrophilic solutes in Mycobacterium chelonei. J. Bacteriol. 172:14181423.
32. Kanetsuna, F. 1968. Chemical analyses of mycobacterial cell walls. Biochim. Biophys. Acta 158:130143.
33. Kartmann, B.,, S. Stenger,, and M. Niederweis. 1999. Porins in the cell wall of Mycobacterium tuberculosis. J. Bacteriol. 181:65436546.
34. Kent, P. W. 1951. Structure of an antigenic polysaccharide isolated from tuberculin J. Chem. Soc. 1:364368.
35. Koebnik, R.,, K. P. Locher,, and P. van Gelder. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:239253.
36. Lemassu, A.,, and M. Daffé. 1994. Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis. Biochem. J. 297:351357.
37. Lemassu, A.,, A. Ortalo-Magné,, F. Bardou,, G. Silve,, M. A. Lanéelle,, and M. Daffé. 1996. Extracellular and surfaceexposed polysaccharides of non-tuberculous mycobacteria. Microbiology 142:15131520.
38. Lichtinger, T.,, B. Heym,, E. Maier,, H. Eichner,, and S. T. Cole. 1999. Evidence for a small anion-selective channel in the cell wall of Mycobacterium bovis BCG besides a wide cationselective pore. FEBS Lett. 454:349355.
39. 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. 271:2954529551.
40. Liu, J.,, E. Y. Rosenberg,, and H. Nikaido. 1995. Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc. Natl. Acad. Sci. USA 92:1125411258.
41. 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. 182:68276830.
42. Minnikin, D. E., 1982. Lipids: complex lipids, their chemistry, biosynthesis and roles, p. 95184. In C. Ratledge, and J. Stanford, (ed.), The Biology of the Mycobacteria, vol. 1. Physiology, Identification and Classification. Academic Press Ltd., London, United Kingdom.
43. Misaki, A.,, and S. Yukawa. 1966. Studies on cell walls of mycobacteria. II. Constitution of polysaccharides from BCG cell walls. J. Biochem. 59:511520.
44. Mizuno, T.,, and S. Mizushima. 1990. Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol. Microbiol. 4:10771082.
45. Mobasheri, H.,, R. H. Senaratne,, P. Draper,, and E. J. A. Lea. 1998. Single channel properties of a porin-like protein from Mycobacterium tuberculosis H37Rv in planar lipid bilayers. Biophys. J. 74:A320.
46. Mukhopadhyay, S.,, D. Basu,, and P. Chakrabarti. 1997. Characterization of a porin from Mycobacterium smegmatis. J. Bacteriol. 179:62056207.
47. Niederweis, M. 2003. Mycobacterial porins new channel proteins in unique outer membranes. Mol. Microbiol. 49: 11671177.
48. Niederweis, M.,, S. Ehrt,, C. Heinz,, U. Klocker,, S. Karosi,, K. M. Swiderek,, L. W. Riley,, and R. Benz. 1999. Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Mol. Microbiol. 33:933945.
49. Nigou, G.,, M. Gilleron,, T. Brando,, A. Vercellone,, and G. Puzo. 1999. Structural definition of arabinomannans from Mycobacterium bovis BCG. Glycoconj. J. 16:257264.
50. Nikaido, H. 1994. Porins and specific diffusion channels in bacterial outer membranes. J. Biol. Chem. 269:39053908.
51. Nikaido, H.,, S. H. Kim,, and E. Y. Rosenberg. 1993. Physical organization of lipids in the cell wall of Mycobacterium chelonae. Mol. Microbiol. 8:10251030.
52. Ohashi, M. 1970. Studies on the chemical structure of serologically active arabinomannan from mycobacteria. Jpn. J. Exp. Med. 40:114.
53. Ortalo-Magné, A.,, M. A. Dupont,, A. Lemassu,, Å. B. Andersen,, P. Gounon,, and M. Daffé. 1995. Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology 141:16091620.
54. Ortalo-Magné, A.,, Å. B. Andersen,, and M. Daffé. 1996. The outermost capsular arabinomannans and other mannoconjugates of virulent and avirulent tubercle bacilli. Microbiology 142:927935.
55. Ortalo-Magné, A.,, A. Lemassu,, M. A. Lanéelle,, F. Bardou,, G. Silve,, P. Gounon,, G. Marchal,, and M. Daffé. 1996. Identification of the surface-exposed lipids on the cell envelope of Mycobacterium tuberculosis and other mycobacterial species. J. Bacteriol. 178:456461.
56. Paul, T. R.,, and T. J. Beveridge. 1992. Reevaluation of envelope profiles and cytoplasmic ultrastructure of mycobacteria processed by conventional embedding and freeze-substitution protocols. J. Bacteriol. 174:65086517.
57. Paul, T. R.,, and T. J. Beveridge. 1994. Preservation of surface lipids and determination of ultrastructure of Mycobacterium kansasii by freeze-substitution. Infect. Immun. 62:15421550.
58. Pautsch, A.,, and G. E. Schulz. 1998. Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol. 5:10131017.
59. 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. 35:478485.
60. Rastogi, N.,, C. Fréhel,, and H. L. David. 1986. Triple-layered structure of mycobacterial cell wall: evidence for the existence of a polysaccharide-rich outer layer in 18 mycobacterial species. Curr. Microbiol. 13:237242.
61. Raynaud, C.,, K. G. Papavinasasundaram,, R. A. Speight,, B. Springer,, P. Sander,, E. Böttger,, M. J. Colston,, and P. Draper. 2002. The functions of OmpATb, a pore-forming protein of Mycobacterium tuberculosis. Mol. Microbiol. 46:191201.
62. Ried, G.,, R. Koebnik,, I. Hindennach,, B. Mutschler,, and U. Henning. 1994. Membrane topology and assembly of outer membrane protein OmpA of Escherichia coli. Mol. Gen. Genet. 243:127135.
63. Saint, N.,, E. De,, N. Julien,, N. Orange,, and G. Molle. 1992. Ionophore properties of OmpA of Escherichia coli. Biochim. Biophys. Acta 1145:119123.
64. Seibert, F. B. 1949. The isolation of three different proteins and two polysaccharides from tuberculin by alcohol fractionation. Their chemical and biological properties. Am. Rev. Tuberc. 59:86101.
65. Senaratne, R. H. 1999. Porin-Like Proteins from Mycobacterium tuberculosis. Ph.D. thesis. Open University, Milton Keynes, United Kingdom.
66. Senaratne, R. H.,, H. Mobasheri,, K. G. Papavinasasundaram,, P. Jenner,, E. J. A. Lea,, and P. Draper. 1998. Expression of a gene for a porin-like protein of the OmpA family from Mycobacterium tuberculosis H37Rv. J. Bacteriol. 180:35413547.
67. Speight, R. A. 2000. The Structure, Function and Regulation of Mycobacterial Porin-Encoding Genes. Ph.D. thesis. University College, London, United Kingdom.
68. Stahl, C.,, S. Kubetzko,, I. Kaps,, S. Seeber,, H. Engelhardt,, and M. Niederweis. 2001. MspA provides the main hydrophobic pathway through the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 40:451464.
69. Sturgill-Koszycki, S.,, P. H. Schlesinger,, P. Chakraborty,, P. L. Hadix,, H. L. Collins,, A. K. Fok,, R. D. Allen,, S. D. Gluck,, J. Heuser,, and D. G. Russell. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678681.
70. Sugawara, E.,, and H. Nikaido. 1992. Pore-forming activity of OmpA porin of Escherichia coli. J. Biol. Chem. 267:25072511.
71. Sugawara, E.,, M. Steiert,, S. Rouhani,, and H. Nikaido. 1996. Secondary structure of the outer membrane proteins OmpA of Escherichia coli and OprF of Pseudomonas aeruginosa. J. Bacteriol. 178:60676069.
72. Trias, J.,, and R. Benz. 1994. Permeability of the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 14:283290.
73. Trias, J.,, V. Jarlier,, and R. Benz. 1992. Porins in the cell wall of mycobacteria. Science 258:14791481.
74. Wang, R.,, M. E. Klegerman,, I. Marsden,, M. Sinnott,, and M. J. Groves. 1995. An anti-neoplastic glycan isolated from Mycobacterium bovis (BCG vaccine). Biochem. J. 311:867872.
75. Wietzerbin, J.,, B. C. Das,, J.-F. Petit,, E. Lederer,, M. Leyh- Bouille,, and J.-M. Ghuysen. 1974. Occurrence of D-alanyl-(D)-meso-diaminopimelic acid and meso-diaminopimelyl-mesodiaminopimelic acid interpeptide linkages in the peptidoglycan of Mycobacteria (sic). Biochemistry 13:34713476.
76. Wietzerbin-Falszpan, J.,, B. C. Das,, I. Azuma,, A. Adam,, J. F. Petit,, and E. Lederer. 1970. Isolation and mass spectrometric identification of the peptide subunits of mycobacterial cell walls. Biochem. Biophys. Res. Commun. 40:5763.
77. Xu, S.,, A. Cooper,, S. Sturgill-Koszycki,, T. van Heyningen,, D. Chatterjee,, I. Orme,, P. Allen,, and D. G. Russell. 1994. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 153:25682578.
78.. Young, D. B.,, J. P. Harnish,, J. Knight,, and T. M. Buchanan. 1985. Detection of phenolic glycolipid I in sera from patients with lepromatous leprosy. J. Infect. Dis. 152:10781081.

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