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

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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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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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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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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: 87 92.
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: 14090 14094.
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: 145 151.
4. Antoine, A. D.,, and B. S. Tepper. 1969. Characterization of glycogen from mycobacteria. Arch. Biochem. Biophys. 134: 207 213.
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: 1594 1600.
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: 501 523.
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: 235 247.
8. Beatty, W. L.,, and D. G. Russell. 2000. Identification of mycobacterial surface proteins released into subcellular compartments of infected macrophages. Infect. Immun. 68: 6997 7002.
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: 31 40.
10. Brennan, P. J.,, and H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64: 29 63.
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: 5251 5255.
12. Brown, I. N.,, and P. Draper. 1976. Growth of Mycobacterium lepraemurium in the mouse bone marrow: an ultrastructural study. Infect. Immun. 13: 1199 1204.
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: 2620 2624.
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: 537 544.
15. Daffé, M.,, and P. Draper. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39: 131 203.
16. Daffé, M.,, and G. Etienne. 1999. The capsule of Mycobacterium tuberculosis and its implications for pathogenicity. Tubercle Lung Dis. 79: 153 169.
17. Daffé, M.,, and A. Lemassu,. 2000. Glycomicrobiology of the mycobacterial cell surface: structure and biological activities of the cell envelope glycoconjugates, p. 225 273. 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: 6734 6743.
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: 383 398.
20. Daniel, T. M., 1984. Soluble mycobacterial antigens, p. 417 465. 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: 12369 12378.
21. Draper, P. 1971. The walls of Mycobacterium lepraemurium: chemistry and ultrastructure. J. Gen. Microbiol. 69: 313 324.
22. Draper, P., 1982. The anatomy of mycobacteria, p. 9 52. 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: 1253 1261.
24. Draper, P.,, O. Kandler,, and A. Darbre. 1987. Peptidoglyacn and arabinogalactan of Mycobacterium leprae. J. Gen Microbiol. 133: 1187 1194.
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: 519 525.
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: 630 637.
27. Engelhardt, H.,, C. Heinz,, and M. Niederweis. 2002. A tetrameric porin limits the cell wall permeability of Mycobacterium smegmatis. J. Biol. Chem. 277: 37567 37572.
27a.. Faller, M.,, M. Niederweis,, and G. E. Schulz. 2004. The structure of a mycobacterial outer-membrane channel. Science 303: 1189 1192.
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: 5437 5442.
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: 8678 8685.
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: 1573 1587.
31. Jarlier, V.,, and H. Nikaido. 1990. Permeability barrier to hydrophilic solutes in Mycobacterium chelonei. J. Bacteriol. 172: 1418 1423.
32. Kanetsuna, F. 1968. Chemical analyses of mycobacterial cell walls. Biochim. Biophys. Acta 158: 130 143.
33. Kartmann, B.,, S. Stenger,, and M. Niederweis. 1999. Porins in the cell wall of Mycobacterium tuberculosis. J. Bacteriol. 181: 6543 6546.
34. Kent, P. W. 1951. Structure of an antigenic polysaccharide isolated from tuberculin J. Chem. Soc. 1: 364 368.
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: 239 253.
36. Lemassu, A.,, and M. Daffé. 1994. Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis. Biochem. J. 297: 351 357.
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: 1513 1520.
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: 349 355.
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: 29545 29551.
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: 11254 11258.
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: 6827 6830.
42. 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 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: 511 520.
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: 1077 1082.
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: 6205 6207.
47. Niederweis, M. 2003. Mycobacterial porins new channel proteins in unique outer membranes. Mol. Microbiol. 49: 1167 1177.
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: 933 945.
49. Nigou, G.,, M. Gilleron,, T. Brando,, A. Vercellone,, and G. Puzo. 1999. Structural definition of arabinomannans from Mycobacterium bovis BCG. Glycoconj. J. 16: 257 264.
50. Nikaido, H. 1994. Porins and specific diffusion channels in bacterial outer membranes. J. Biol. Chem. 269: 3905 3908.
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: 1025 1030.
52. Ohashi, M. 1970. Studies on the chemical structure of serologically active arabinomannan from mycobacteria. Jpn. J. Exp. Med. 40: 1 14.
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: 1609 1620.
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: 927 935.
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: 456 461.
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: 6508 6517.
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: 1542 1550.
58. Pautsch, A.,, and G. E. Schulz. 1998. Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol. 5: 1013 1017.
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: 478 485.
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: 237 242.
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 OmpA Tb, a pore-forming protein of Mycobacterium tuberculosis. Mol. Microbiol. 46: 191 201.
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: 127 135.
63. Saint, N.,, E. De,, N. Julien,, N. Orange,, and G. Molle. 1992. Ionophore properties of OmpA of Escherichia coli. Biochim. Biophys. Acta 1145: 119 123.
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: 86 101.
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: 3541 3547.
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: 451 464.
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: 678 681.
70. Sugawara, E.,, and H. Nikaido. 1992. Pore-forming activity of OmpA porin of Escherichia coli. J. Biol. Chem. 267: 2507 2511.
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: 6067 6069.
72. Trias, J.,, and R. Benz. 1994. Permeability of the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 14: 283 290.
73. Trias, J.,, V. Jarlier,, and R. Benz. 1992. Porins in the cell wall of mycobacteria. Science 258: 1479 1481.
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: 867 872.
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: 3471 3476.
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: 57 63.
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: 2568 2578.
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: 1078 1081.

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